Skip to main content

Advertisement

SpringerLink
Log in

The Expanding Spectrum of Human coronin 1A deficiency

  • Immune Deficiency and Dysregulation (DP Huston, Section Editor)
  • Published:
Current Allergy and Asthma Reports Aims and scope Submit manuscript

Abstract

Since the first discovery of coronin in the amoeba Dictyostelium discoideum, remarkable insights have been gained regarding the structure and function of coronins, highly conserved from yeast to humans. It has been speculated that coronins have evolved from actin-binding molecules in lower eukaryotes to regulators of various cellular processes in mammals. Indeed, coronins are not only involved in cytokinesis, cell motility, and other actin-related processes but they are also implicated in immune homeostasis and calcium–calcineurin signaling. Most strikingly, coronin 1 deficiencies give rise to immune deficiencies in mice and humans that are characterized by severe T lymphocytopenia. Whereas complete absence of coronin 1A is associated with severe combined immunodeficiency in humans, hypomorphic mutations lead to a profound defect in naïve T cells, expansion of oligoclonal memory T cells, and exquisite susceptibility to EBV-associated B cell lymphoproliferation. Recent publications show that coronin 1A also plays a role in natural killer cell cytotoxic function and in neurobehavioral processes. It can be expected that future identification of coronin 1A-deficient patients will further extend the phenotypic spectrum thereby increasing our knowledge of this fascinating molecule.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 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.

    PubMed Central  PubMed  Google Scholar 

  2. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. de Hostos EL, Rehfuess C, Bradtke B, et al. Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J Cell Biol. 1993;120(1):163–73.

    Article  PubMed  Google Scholar 

  4. Eckert C, Hammesfahr B, Kollmar M. A holistic phylogeny of the coronin gene family reveals an ancient origin of the tandem-coronin, defines a new subfamily, and predicts protein function. BMC Evol Biol. 2011;11:268.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Xavier CP, Eichinger L, Fernandez MP, Morgan RO, Clemen CS. Evolutionary and functional diversity of coronin proteins. Sub-cellular Biochem. 2008;48:98–109.

    Article  Google Scholar 

  6. de Hostos EL. The coronin family of actin-associated proteins. Trends Cell Biol. 1999;9(9):345–50.

    Article  PubMed  Google Scholar 

  7. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Kammerer RA, Kostrewa D, Progias P, et al. A conserved trimerization motif controls the topology of short coiled coils. Proc Natl Acad Sci U S A. 2005;102(39):13891–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. 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.

    Article  CAS  PubMed  Google Scholar 

  10. Rybakin V, Stumpf M, Schulze A, Majoul IV, Noegel AA, Hasse A. Coronin 7, the mammalian POD-1 homologue, localizes to the Golgi apparatus. FEBS Lett. 2004;573(1–3):161–7.

    Article  CAS  PubMed  Google Scholar 

  11. Suzuki K, Nishihata J, Arai Y, 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.

    Article  CAS  PubMed  Google Scholar 

  12. Oku T, Itoh S, Okano M, et al. Two regions responsible for the actin binding of p57, a mammalian coronin family actin-binding protein. Biol Pharm Bull. 2003;26(4):409–16.

    Article  PubMed  Google Scholar 

  13. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.

    Article  CAS  PubMed  Google Scholar 

  14. Rybakin V, Clemen CS. Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. BioEssays News Rev Mol Cell Dev Biol. 2005;27(6):625–32.

    Article  CAS  Google Scholar 

  15. 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.

    Article  PubMed  Google Scholar 

  16. Huang W, Ghisletti S, Saijo K, et al. Coronin 2A mediates actin-dependent de-repression of inflammatory response genes. Nature. 2011;470(7334):414–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Cai L, Makhov AM, Bear JE. F-actin binding is essential for coronin 1B function in vivo. J Cell Sci. 2007;120(Pt 10):1779–90.

    Article  CAS  PubMed  Google Scholar 

  18. Cai L, Marshall TW, Uetrecht AC, Schafer DA, Bear JE. Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell. 2007;128(5):915–29.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Pieters J, Muller P, Jayachandran R. On guard: coronin proteins in innate and adaptive immunity. Nat Rev Immunol. 2014;13(7):510–8. A very recent and comprehensive review on the coronin proteins and the many facettes of their functions.

    Article  Google Scholar 

  20. 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.

    Article  CAS  PubMed  Google Scholar 

  21. Jayachandran R, Sundaramurthy V, Combaluzier B, et al. Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. Cell. 2007;130(1):37–50.

    Article  CAS  PubMed  Google Scholar 

  22. Suzuki K, Takeshita F, Nakata N, Ishii N, Makino M. Localization of CORO1A in the macrophages containing Mycobacterium leprae. Acta Histochem Cytochemica. 2006;39(4):107–12.

    Article  CAS  Google Scholar 

  23. Zheng PY, Jones NL. Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein. Cell Microbiol. 2003;5(1):25–40.

    Article  CAS  PubMed  Google Scholar 

  24. Combaluzier B, Pieters J. Chemotaxis and phagocytosis in neutrophils is independent of coronin 1. J Immunol. 2009;182(5):2745–52.

    Article  CAS  PubMed  Google Scholar 

  25. Westritschnig K, BoseDasgupta S, Tchang V, Siegmund K, Pieters J. Antigen processing and presentation by dendritic cells is independent of coronin 1. Mol Immunol. 2013;53(4):379–86. First report on the role of coronin 1 in dendritic cells.

    Article  CAS  PubMed  Google Scholar 

  26. Haraldsson MK, Louis-Dit-Sully CA, Lawson BR, et al. The lupus-related Lmb3 locus contains a disease-suppressing Coronin-1A gene mutation. Immunity. 2008;28(1):40–51.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Mueller P, Massner J, Jayachandran R, 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.

    Article  CAS  PubMed  Google Scholar 

  28. Mugnier B, Nal B, Verthuy C, et al. Coronin-1A links cytoskeleton dynamics to TCR alpha beta-induced cell signaling. PLoS One. 2008;3(10):e3467.

    Article  PubMed Central  PubMed  Google Scholar 

  29. Shiow LR, Roadcap DW, Paris K, 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  31. 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Moshous D, Martin E, Carpentier W, 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. In this study, the second kindred with CORO1A deficiency is described. The patients, three siblings, presented a hypomorphic mutation in Coro1a leading to a combined immunodeficiency and particular predisposition to develop EBV-associated B-cell lymphoproliferation at an very early age.

    Article  CAS  PubMed  Google Scholar 

  33. Hogquist KA. Immunodeficiency: when T cells are stuck at home. Nat Immunol. 2008;9(11):1207–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Yagi H, Matsumoto M, Nakamura M, et al. Defect of thymocyte emigration in a T cell deficiency strain (CTS) of the mouse. J Immunol. 1996;157(8):3412–9.

    CAS  PubMed  Google Scholar 

  35. Engelhardt KR, McGhee S, Winkler S, et al. Large deletions and point mutations involving the dedicator of cytokinesis 8 (DOCK8) in the autosomal-recessive form of hyper-IgE syndrome. J Allergy Clin Immunol. 2009;124(6):1289–302 e4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Nehme NT, Pachlopnik Schmid J, Debeurme F, et al. MST1 mutations in autosomal recessive primary immunodeficiency characterized by defective naive T-cell survival. Blood. 2012;119(15):3458–68.

    Article  CAS  PubMed  Google Scholar 

  37. Abdollahpour H, Appaswamy G, Kotlarz D, et al. The phenotype of human STK4 deficiency. Blood. 2012;119(15):3450–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Mou F, Praskova M, Xia F, et al. The Mst1 and Mst2 kinases control activation of rho family GTPases and thymic egress of mature thymocytes. J Exp Med. 2012;209(4):741–59.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. 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. This is the first report on the role of Coronin 1A for NK cell function.

    Article  CAS  PubMed  Google Scholar 

  40. Jayachandran R, Liu X, Bosedasgupta S, et al. Coronin 1 regulates cognition and behavior through modulation of cAMP/protein kinase A signaling. PLoS Biol. 2014;12(3):e1001820. Important work showing the critical role for coronin 1 in neurobehavior in mice and humans through regulating the transmission of signals within cells. It is shown that coronin 1 modulates the cyclic adenosine monophosphate (cAMP) and protein kinase A (PKA) signaling.

    Article  PubMed Central  PubMed  Google Scholar 

  41. Weiss LA, Shen Y, Korn JM, et al. Association between microdeletion and microduplication at 16p11.2 and autism. N Engl J Med. 2008;358(7):667–75.

    Article  CAS  PubMed  Google Scholar 

  42. Rosenfeld JA, Coppinger J, Bejjani BA, Girirajan S, Eichler EE. Speech delays and behavioral problems are the predominant features in individuals with developmental delays and 16p11.2 microdeletions and microduplications. J Neurodev Disord. 2010;2:26–38.

    Article  PubMed Central  PubMed  Google Scholar 

  43. Kumar RA, KaraMohamed S, Sudi J, et al. Recurrent 16p11.2 microdeletions in autism. Hum Mol Genet. 2008;17(4):628–38.

    Article  CAS  PubMed  Google Scholar 

  44. Shinawi M, Liu P, Kang SH, et al. Recurrent reciprocal 16p11.2 rearrangements associated with global developmental delay, behavioural problems, dysmorphism, epilepsy, and abnormal head size. J Med Genet. 2010;47(5):332–41.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Shen Z, Zhang X, Chai Y, et al. Conditional knockouts generated by engineered crispr-cas9 endonuclease reveal the roles of coronin in C. elegans neural development. Dev Cell. 2014. doi:10.1016/j.devcel.2014.07.017. A very recent study showing very elegantly through a conditional knockout strategy that Coronin is implicated in regulation of actin organization and cell morphology during postembryonic neuroblast migration and neuritogenesis in C. elegans.

    Google Scholar 

  46. Shiow LR, Paris K, Puck JM. Severe combined immunodeficiency due to absent coronin-1a. Primary immunodeficiency diseases a molecular and genetic approach 2014; 3rd ed. In: Ochs HD, Smith E, and Puck, JM, editors. 295.

  47. Okumura M, Kung C, Wong S, Rodgers M, Thomas ML. Definition of family of coronin-related proteins conserved between humans and mice: close genetic linkage between coronin-2 and CD45-associated protein. DNA Cell Biol. 1998;17(9):779–87.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by institutional grants from INSERM, Ligue Nationale contre le Cancer (Equipe Labellisée La Ligue), INCa, Institut Imagine, and the European Research Council (PIDIMMUN grant no. 249816).

Compliance with Ethics Guidelines

ᅟ

Conflict of Interest

Despina Moshous and Jean-Pierre de Villartay report no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by the authors.

Author information

Authors and Affiliations

  1. INSERM UMR1163, Genome Dynamics in the Immune System, Paris, France

    Despina Moshous & Jean-Pierre de Villartay

  2. Université Paris Descartes—Sorbonne Paris Cité, Institut Imagine, 24 Boulevard du Montparnasse, 75015, Paris, France

    Despina Moshous & Jean-Pierre de Villartay

  3. AP-HP, Hôpital Necker–Enfants Malades, Unité d’Immunologie, Hématologie et Rhumatologie Pédiatriques, 149, rue de Sèvres, 75015, Paris, France

    Despina Moshous

Authors
  1. Despina Moshous
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Pierre de Villartay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Despina Moshous.

Additional information

This article is part of the Topical Collection on Immune Deficiency and Dysregulation

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moshous, D., de Villartay, JP. The Expanding Spectrum of Human coronin 1A deficiency. Curr Allergy Asthma Rep 14, 481 (2014). https://doi.org/10.1007/s11882-014-0481-1

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11882-014-0481-1

Keywords

Search

Navigation