Advertisement

Journal of Clinical Immunology

, Volume 35, Issue 2, pp 100–107 | Cite as

Coronin-1A: Immune Deficiency in Humans and Mice

  • Divya Punwani
  • Barry Pelz
  • Jason Yu
  • Nicoleta C. Arva
  • Kristian Schafernak
  • Karly Kondratowicz
  • Melanie MakhijaEmail author
  • Jennifer M. PuckEmail author
CME Review

Introduction

The study of human primary immunodeficiencies (PIDs) has identified factors critical for the development and function of the immune system [1]. While typical severe combined immunodeficiency (SCID) in humans is defined by a profound block in T lymphocyte production, with or without associated B and NK lymphocyte defects, more heterogeneous combined immunodeficiency (CID) disorders arise from gene defects that allow T lymphocytes to mature, but hinder their survival, release from the thymus into the periphery, or effector functions [2]. Individuals with CID may have both impairment of immune responses and defects in immune regulation; thus they may experience severe, recurrent and opportunistic infections as well as autoimmune disorders [3, 4].

Members of the coronin family of proteins are important regulators of the actin cytoskeleton, and mutations in CORO1A, encoding Coronin-1A, the predominant coronin expressed in lymphocytes, cause variable degrees of T cell...

Keywords

Chromosome 16p11.2 combined immunodeficiency (CID) immune dysregulation epstein-barr virus (EBV) primary immunodeficiency thymus 

References

  1. 1.
    Milner JD, Holland SM. The cup runneth over: lessons from the ever-expanding pool of primary immunodeficiency diseases. Nat Rev Immunol. 2013;13(9):635–48. doi: 10.1038/nri3493.CrossRefPubMedGoogle Scholar
  2. 2.
    Al-Herz W, Bousfiha A, Casanova JL, Chatila T, Conley ME, Cunningham-Rundles C, et al. Primary immunodeficiency diseases: an update on the classification from the international union of immunological societies expert committee for primary immunodeficiency. Front Immunol. 2014;5:162. doi: 10.3389/fimmu.2014.00162.PubMedCentralPubMedGoogle Scholar
  3. 3.
    Liston A, Enders A, Siggs OM. Unravelling the association of partial T-cell immunodeficiency and immune dysregulation. Nat Rev Immunol. 2008;8(7):545–58. doi: 10.1038/nri2336.CrossRefPubMedGoogle Scholar
  4. 4.
    Notarangelo LD. Functional T, cell immunodeficiencies (with T cells present). Annu Rev Immunol. 2013;31:195–225. doi: 10.1146/annurev-immunol-032712-095927.CrossRefPubMedGoogle Scholar
  5. 5.
    Shiow LR, Roadcap DW, Paris K, Watson SR, Grigorova IL, Lebet T, et al. The actin regulator coronin 1A is mutant in a thymic egress-deficient mouse strain and in a patient with severe combined immunodeficiency. Nat Immunol. 2008;9(11):1307–15. doi: 10.1038/ni.1662.CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    Shiow LR, Paris K, Akana MC, Cyster JG, Sorensen RU, Puck JM. Severe combined immunodeficiency (SCID) and attention deficit hyperactivity disorder (ADHD) associated with a Coronin-1A mutation and a chromosome 16p11.2 deletion. Clin Immunol. 2009;131(1):24–30. doi: 10.1016/j.clim.2008.11.002.CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Moshous D, Martin E, Carpentier W, Lim A, Callebaut I, Canioni D, et al. Whole-exome sequencing identifies Coronin-1A deficiency in 3 siblings with immunodeficiency and EBV-associated B-cell lymphoproliferation. J Allergy Clin Immunol. 2013;131(6):1594–603. doi: 10.1016/j.jaci.2013.01.042.CrossRefPubMedGoogle Scholar
  8. 8.
    Rouwette M, Noben JP, Van Horssen J, Van Wijmeersch B, Hupperts R, Jongen PJ, et al. Identification of coronin-1a as a novel antibody target for clinically isolated syndrome and multiple sclerosis. J Neurochem. 2013;126(4):483–92. doi: 10.1111/jnc.12335.CrossRefPubMedGoogle Scholar
  9. 9.
    Xu XJ, Tang YM, Zhao HZ, Guo L, Wang ZJ. ZCH-2B8a, an antibody targeting actin-binding protein coronin-1a, is a potential therapeutic agent for B-lineage malignancies. J Drug Target. 2014. doi: 10.3109/1061186X.2014.888072.Google Scholar
  10. 10.
    de Hostos EL, Bradtke B, Lottspeich F, Guggenheim R, Gerisch G. Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein beta subunits. EMBO J. 1991;10(13):4097–104.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Suzuki K, Nishihata J, Arai Y, Honma N, Yamamoto K, Irimura T, et al. Molecular cloning of a novel actin-binding protein, p57, with a WD repeat and a leucine zipper motif. FEBS Lett. 1995;364(3):283–8.CrossRefPubMedGoogle Scholar
  12. 12.
    Jayachandran R, Gatfield J, Massner J, Albrecht I, Zanolari B, Pieters J. RNA interference in J774 macrophages reveals a role for coronin 1 in mycobacterial trafficking but not in actin-dependent processes. Mol Biol Cell. 2008;19(3):1241–51. doi: 10.1091/mbc.E07-07-0640.CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Jayachandran R, Sundaramurthy V, Combaluzier B, Mueller P, Korf H, Huygen K, et al. Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. Cell. 2007;130(1):37–50. doi: 10.1016/j.cell.2007.04.043.CrossRefPubMedGoogle Scholar
  14. 14.
    Mueller P, Massner J, Jayachandran R, Combaluzier B, Albrecht I, Gatfield J, et al. Regulation of T cell survival through coronin-1-mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering. Nat Immunol. 2008;9(4):424–31. doi: 10.1038/ni1570.CrossRefPubMedGoogle Scholar
  15. 15.
    Yagi H, Matsumoto M, Nakamura M, Makino S, Suzuki R, Harada M, et al. Defect of thymocyte emigration in a T cell deficiency strain (CTS) of the mouse. J Immunol. 1996;157(8):3412–9.PubMedGoogle Scholar
  16. 16.
    Haraldsson MK, Louis-Dit-Sully CA, Lawson BR, Sternik G, Santiago-Raber ML, Gascoigne NR, et al. The lupus-related Lmb3 locus contains a disease-suppressing Coronin-1A gene mutation. Immunity. 2008;28(1):40–51. doi: 10.1016/j.immuni.2007.11.023.CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Foger N, Rangell L, Danilenko DM, Chan AC. Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science. 2006;313(5788):839–42. doi: 10.1126/science.1130563.CrossRefPubMedGoogle Scholar
  18. 18.
    Mace EM, Orange JS. Lytic immune synapse function requires filamentous actin deconstruction by Coronin 1A. Proc Natl Acad Sci U S A. 2014;111(18):6708–13. doi: 10.1073/pnas.1314975111.CrossRefPubMedCentralPubMedGoogle Scholar
  19. 19.
    Stray-Pedersen A, Jouanguy E, Crequer A, Bertuch AA, Brown BS, Jhangiani SN, et al. Compound Heterozygous CORO1A Mutations in Siblings with a Mucocutaneous-Immunodeficiency Syndrome of Epidermodysplasia Verruciformis-HPV, Molluscum Contagiosum and Granulomatous Tuberculoid Leprosy. J Clin Immunol. 2014;34(7):871–90. doi: 10.1007/s10875-014-0074-8.CrossRefPubMedGoogle Scholar
  20. 20.
    de Hostos EL. The coronin family of actin-associated proteins. Trends Cell Biol. 1999;9(9):345–50.CrossRefPubMedGoogle Scholar
  21. 21.
    Ferrari G, Langen H, Naito M, Pieters J. A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell. 1999;97(4):435–47.CrossRefPubMedGoogle Scholar
  22. 22.
    Nal B, Carroll P, Mohr E, Verthuy C, Da Silva MI, Gayet O, et al. Coronin-1 expression in T lymphocytes: insights into protein function during T cell development and activation. Int Immunol. 2004;16(2):231–40.CrossRefPubMedGoogle Scholar
  23. 23.
    Appleton BA, Wu P, Wiesmann C. The crystal structure of murine coronin-1: a regulator of actin cytoskeletal dynamics in lymphocytes. Structure. 2006;14(1):87–96. doi: 10.1016/j.str.2005.09.013.CrossRefPubMedGoogle Scholar
  24. 24.
    Gatfield J, Albrecht I, Zanolari B, Steinmetz MO, Pieters J. Association of the leukocyte plasma membrane with the actin cytoskeleton through coiled coil-mediated trimeric coronin 1 molecules. Mol Biol Cell. 2005;16(6):2786–98. doi: 10.1091/mbc.E05-01-0042.CrossRefPubMedCentralPubMedGoogle Scholar
  25. 25.
    Rybakin V, Clemen CS. Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. BioEssays: News and Rev Mol, Cell Dev Biol. 2005;27(6):625–32. doi: 10.1002/bies.20235.CrossRefGoogle Scholar
  26. 26.
    Uetrecht AC, Bear JE. Coronins: the return of the crown. Trends Cell Biol. 2006;16(8):421–6. doi: 10.1016/j.tcb.2006.06.002.CrossRefPubMedGoogle Scholar
  27. 27.
    Machesky LM, Reeves E, Wientjes F, Mattheyse FJ, Grogan A, Totty NF, et al. Mammalian actin-related protein 2/3 complex localizes to regions of lamellipodial protrusion and is composed of evolutionarily conserved proteins. Biochem J. 1997;328(Pt 1):105–12.PubMedCentralPubMedGoogle Scholar
  28. 28.
    Humphries CL, Balcer HI, D’Agostino JL, Winsor B, Drubin DG, Barnes G, et al. Direct regulation of Arp2/3 complex activity and function by the actin binding protein coronin. J Cell Biol. 2002;159(6):993–1004. doi: 10.1083/jcb.200206113.CrossRefPubMedCentralPubMedGoogle Scholar
  29. 29.
    Rodal AA, Sokolova O, Robins DB, Daugherty KM, Hippenmeyer S, Riezman H, et al. Conformational changes in the Arp2/3 complex leading to actin nucleation. Nat Struct Mol Biol. 2005;12(1):26–31. doi: 10.1038/nsmb870.CrossRefPubMedGoogle Scholar
  30. 30.
    Mueller P, Liu X, Pieters J. Migration and homeostasis of naive T cells depends on coronin 1-mediated prosurvival signals and not on coronin 1-dependent filamentous actin modulation. J Immunol. 2011;186(7):4039–50. doi: 10.4049/jimmunol.1003352.CrossRefPubMedGoogle Scholar
  31. 31.
    Kueh HY, Charras GT, Mitchison TJ, Brieher WM. Actin disassembly by cofilin, coronin, and Aip1 occurs in bursts and is inhibited by barbed-end cappers. J Cell Biol. 2008;182(2):341–53. doi: 10.1083/jcb.200801027.CrossRefPubMedCentralPubMedGoogle Scholar
  32. 32.
    Gandhi M, Achard V, Blanchoin L, Goode BL. Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Mol Cell. 2009;34(3):364–74. doi: 10.1016/j.molcel.2009.02.029.CrossRefPubMedCentralPubMedGoogle Scholar
  33. 33.
    Chan KT, Creed SJ, Bear JE. Unraveling the enigma: progress towards understanding the coronin family of actin regulators. Trends Cell Biol. 2011;21(8):481–8. doi: 10.1016/j.tcb.2011.04.004.CrossRefPubMedCentralPubMedGoogle Scholar
  34. 34.
    Brieher WM, Kueh HY, Ballif BA, Mitchison TJ. Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J Cell Biol. 2006;175(2):315–24. doi: 10.1083/jcb.200603149.CrossRefPubMedCentralPubMedGoogle Scholar
  35. 35.
    Castro-Castro A, Ojeda V, Barreira M, Sauzeau V, Navarro-Lerida I, Muriel O, et al. Coronin 1A promotes a cytoskeletal-based feedback loop that facilitates Rac1 translocation and activation. EMBO J. 2011;30(19):3913–27. doi: 10.1038/emboj.2011.310.CrossRefPubMedCentralPubMedGoogle Scholar
  36. 36.
    Pieters J, Muller P, Jayachandran R. On guard: coronin proteins in innate and adaptive immunity. Nat Rev Immunol. 2013;13(7):510–8. doi: 10.1038/nri3465.CrossRefPubMedGoogle Scholar
  37. 37.
    Ichikawa D, Mizuno M, Yamamura T, Miyake S. GRAIL (gene related to anergy in lymphocytes) regulates cytoskeletal reorganization through ubiquitination and degradation of Arp2/3 subunit 5 and coronin 1A. J Biol Chem. 2011;286(50):43465–74. doi: 10.1074/jbc.M111.222711.CrossRefPubMedCentralPubMedGoogle Scholar
  38. 38.
    Tchang VS, Mekker A, Siegmund K, Karrer U, Pieters J. Diverging role for coronin 1 in antiviral CD4 + and CD8 + T cell responses. Mol Immunol. 2013;56(4):683–92. doi: 10.1016/j.molimm.2013.05.003.CrossRefPubMedGoogle Scholar
  39. 39.
    Jayachandran R, Liu X, Bosedasgupta S, Muller P, Zhang CL, Moshous D, et al. Coronin 1 regulates cognition and behavior through modulation of cAMP/protein kinase A signaling. PLoS Biol. 2014;12(3):e1001820. doi: 10.1371/journal.pbio.1001820.CrossRefPubMedCentralPubMedGoogle Scholar
  40. 40.
    Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7(4):248–9. doi: 10.1038/nmeth0410-248.CrossRefPubMedCentralPubMedGoogle Scholar
  41. 41.
    Moshous D, de Villartay JP. The expanding spectrum of human coronin 1A deficiency. Curr Allergy Asthma Rep. 2014;14(12):481. doi: 10.1007/s11882-014-0481-1.CrossRefPubMedGoogle Scholar
  42. 42.
    Parvaneh N, Filipovich AH, Borkhardt A. Primary immunodeficiencies predisposed to Epstein-Barr virus-driven haematological diseases. Br J Haematol. 2013;162(5):573–86. doi: 10.1111/bjh.12422.CrossRefPubMedGoogle Scholar
  43. 43.
    Hogquist KA. Immunodeficiency: when T cells are stuck at home. Nat Immunol. 2008;9(11):1207–8. doi: 10.1038/ni1108-1207.CrossRefPubMedCentralPubMedGoogle Scholar
  44. 44.
    Weiss LA, Shen Y, Korn JM, Arking DE, Miller DT, Fossdal R, et al. Association between microdeletion and microduplication at 16p11.2 and autism. N Engl J Med. 2008;358(7):667–75. doi: 10.1056/NEJMoa075974.CrossRefPubMedGoogle Scholar
  45. 45.
    Horev G, Ellegood J, Lerch JP, Son YE, Muthuswamy L, Vogel H, et al. Dosage-dependent phenotypes in models of 16p11.2 lesions found in autism. Proc Natl Acad Sci U S A. 2011;108(41):17076–81. doi: 10.1073/pnas.1114042108.CrossRefPubMedCentralPubMedGoogle Scholar
  46. 46.
    Kaminski S, Hermann-Kleiter N, Meisel M, Thuille N, Cronin S, Hara H, et al. Coronin 1A is an essential regulator of the TGFbeta receptor/SMAD3 signaling pathway in Th17 CD4(+) T cells. J Autoimmun. 2011;37(3):198–208. doi: 10.1016/j.jaut.2011.05.018.CrossRefPubMedGoogle Scholar
  47. 47.
    Siegmund K, Zeis T, Kunz G, Rolink T, Schaeren-Wiemers N, Pieters J. Coronin 1-mediated naive T cell survival is essential for the development of autoimmune encephalomyelitis. J Immunol. 2011;186(6):3452–61. doi: 10.4049/jimmunol.1003491.CrossRefPubMedGoogle Scholar
  48. 48.
    Rouwette M, Somers K, Govarts C, De Deyn PP, Hupperts R, Van Wijmeersch B, et al. Novel cerebrospinal fluid and serum autoantibody targets for clinically isolated syndrome. J Neurochem. 2012;123(4):568–77. doi: 10.1111/jnc.12005.CrossRefPubMedGoogle Scholar
  49. 49.
    Xu XJ, Tang YM. Coronin-1a is a potential therapeutic target for activated T cell-related immune disorders. APMIS. 2014. doi: 10.1111/apm.12277.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Divya Punwani
    • 1
  • Barry Pelz
    • 2
  • Jason Yu
    • 1
  • Nicoleta C. Arva
    • 3
  • Kristian Schafernak
    • 3
  • Karly Kondratowicz
    • 1
  • Melanie Makhija
    • 2
    Email author
  • Jennifer M. Puck
    • 1
    Email author
  1. 1.Department of PediatricsUniversity of California San Francisco and UCSF Benioff Children’s HospitalSan FranciscoUSA
  2. 2.Division of Allergy & Immunology, Department of Pediatrics, Ann & Robert H. Lurie Children’s Hospital of ChicagoNorthwestern UniversityChicagoUSA
  3. 3.Department of Pathology and Laboratory Medicine, Ann & Robert H. Lurie Children’s Hospital of ChicagoNorthwestern UniversityChicagoUSA

Personalised recommendations