The actin-bundling protein L-plastin: A critical regulator of immune cell function

International Journal of Cell Biology

Volumn , Issue , 2012, Pages

  Morley, Sharon Celeste ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTANOL; CALCIUM; CELL PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; F ACTIN; FC RECEPTOR; FORMYLMETHIONYLLEUCYLPHENYLALANINE; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR LIKE 1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; INTEGRIN; INTERLEUKIN 1; INTERLEUKIN 2; L PLASTIN PROTEIN; LIPOPOLYSACCHARIDE; LYMPHOCYTE ANTIGEN RECEPTOR; MACROPHAGE MIGRATION INHIBITION FACTOR; PHORBOL 12 ACETATE 13 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE D; PROTEIN KINASE C; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WORTMANNIN;

B LYMPHOCYTE; CELL ADHESION; CELL FUNCTION; CELL MOTILITY; CELL PHAGOCYTOSIS; CELL TRANSFORMATION; CELL TYPE; ENZYME REGULATION; EOSINOPHIL; FIBROBLAST; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL SYNAPSE; IN VITRO STUDY; MACROPHAGE MIGRATION; NEUTROPHIL; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; T LYMPHOCYTE;

EID: 84855602449     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2012/935173     Document Type: Review

References (92)

1. Samstag Y., Eibert S. M., Klemke M., Wabnitz G. H., Actin cytoskeletal dynamics in T lymphocyte activation and migration Journal of Leukocyte Biology 2003 73 1 30 48 (Pubitemid 36125673)
2. Dustin M. L., Hunter to gatherer and back: immunological synapses and kinapses as variations on the theme of amoeboid locomotion Annual Review of Cell and Developmental Biology 2008 24 577 596
3. Gomez T. S., Billadeau D. D., T cell activation and the cytoskeleton: you can't have one without the other Advances in Immunology 2008 97 1 64 (Pubitemid 351711631)
4. Beemiller P., Krummel M. F., Mediation of T-cell activation by actin meshworks Cold Spring Harbor perspectives in biology 2010 2 9 a002444
5. Imhof B. A., Aurrand-Lions M., Adhesion mechanisms regulating the migration of monocytes Nature Reviews Immunology 2004 4 6 432 444 (Pubitemid 38745555)
6. Vicente-Manzanares M., Webb D. J., Horwitz A. R., Cell migration at a glance Journal of Cell Science 2005 118 21 4917 4919 (Pubitemid 41672422)
7. Kehrl J. H., Chemoattractant receptor signaling and the control of lymphocyte migration Immunologic Research 2006 34 3 211 227 (Pubitemid 44195937)
8. Kehrl J. H., Hwang I. Y., Park C., Chemoattract receptor signaling and its role in lymphocyte motility and trafficking Current Topics in Microbiology and Immunology 2009 334 1 107 127
9. Worbs T., Forster R., T cell migration dynamics within lymph nodes during steady state: an overview of extracellular and intracellular factors influencing the basal intranodal T cell motility Current Topics in Microbiology and Immunology 2009 334 1 71 105
10. Weber M., Sixt M., MEK signalling tunes actin treadmilling for interstitial lymphocyte migration The EMBO Journal 2010 29 17 2861 2863
11. Niedergang F., Chavrier P., Regulation of phagocytosis by Rho GTPases Current Topics in Microbiology and Immunology 2005 291 43 60 (Pubitemid 40674910)
12. Radulovic M., Godovac-Zimmermann J., Proteomic approaches to understanding the role of the cytoskeleton in host-defense mechanisms Expert Review of Proteomics 2011 8 1 117 126
13. Adams A. E., Shen W., Lin C. S., Leavitt J., Matsudaira P., Isoform-specific complementation of the yeast sac6 null mutation by human fimbrin Molecular and Cellular Biology 1995 15 1 69 75 (Pubitemid 24379902)
14. Goldstein D., Djeu J., Latter G., Abundant synthesis of the transformation-induced protein of neoplastic human fibroblasts, plastin, in normal lymphocytes Cancer Research 1985 45 11, part 2 5643 5647 (Pubitemid 16218567)
15. Lin C. S., Aebersold R. H., Kent S. B., Varma M., Leavitt J., Molecular cloning and characterization of plastin, a human leukocyte protein expressed in transformed human fibroblasts Molecular and Cellular Biology 1988 8 11 4659 4668 (Pubitemid 18261543)
16. de Arruda M. V., Watson S., Lin C. S., Leavitt J., Matsudaira P., Fimbrin is a homologue of the cytoplasmic phosphoprotein plastin and has domains homologous with calmodulin and actin gelation proteins Journal of Cell Biology 1990 111 3 1069 1079
17. Pacaud M., Purification and further characterization of macrophage 70-kDa protein, a calcium-regulated, actin-binding protein identical to L-plastin Biochemistry 1993 32 13 3448 3455 (Pubitemid 23126914)
18. Lin C. S., Park T., Chen Z. P., Leavitt J., Human plastin genes. Comparative gene structure, chromosome location, and differential expression in normal and neoplastic cells Journal of Biological Chemistry 1993 268 4 2781 2792 (Pubitemid 23057910)
19. Lin C. S., Shen W., Chen Z. P., Tu Y. H., Matsudaira P., Identification of I-plastin, a human fimbrin isoform expressed in intestine and kidney Molecular and Cellular Biology 1994 14 4 2457 2467 (Pubitemid 24108228)
20. Delanote V., Vandekerckhove J., Gettemans J., Plastins: versatile modulators of actin organization in (patho)physiological cellular processes Acta Pharmacologica Sinica 2005 26 7 769 779 (Pubitemid 40978757)
21. le Goff E., Vallentin A., Harmand P. O., Aldrian-Herrada G., Rebire B., Roy C., Benyamin Y., Lebart M. C., Characterization of L-plastin Interaction with beta integrin and its regulation by micro-calpain Cytoskeleton 2010 67 5 286 296
22. Shinomiya H., Shinjo M., Fengzhi L., Asano Y., Kihara H., Conformational analysis of the leukocyte-specific EF-hand protein p65/L-plastin by X-ray scattering in solution Biophysical Chemistry 2007 131 13 36 42 (Pubitemid 350030358)
23. Hanein D., Volkmann N., Goldsmith S., Michon A. M., Lehman W., Craig R., DeRosier D., Almo S., Matsudaira P., An atomic model of fimbrin binding to F-actin and its implications for filament crosslinking and regulation Nature Structural Biology 1998 5 9 787 792 (Pubitemid 28402082)
24. Volkmann N., Derosier D., Matsudaira P., Hanein D., An atomic model of actin filaments cross-linked by fimbrin and its implications for bundle assembly and function The Journal of Cell Biology 2001 153 5 947 956 (Pubitemid 34289235)
25. Galkin V. E., Orlova A., Cherepanova O., Lebart M. C., Egelman E. H., High-resolution cryo-EM structure of the F-actin-fimbrin/plastin ABD2 complex Proceedings of the National Academy of Sciences of the United States of America 2008 105 5 1494 1498 (Pubitemid 351346542)
26. Lebart M. C., Hubert F., Boiteau C., Ventéo S., Roustan C., Benyamin Y., Biochemical characterization of the L-plastin-actin interaction shows a resemblance with that of -actinin and allows a distinction to be made between the two actin-binding domains of the molecule Biochemistry 2004 43 9 2428 2437 (Pubitemid 38327838)
27. Anderson N. L., Gemmell M. A., Coussens P. M., Specific protein phosphorylation in human promyelocytic HL-60 leukemia cells susceptible or resistant to induction of cell differentiation by phorbol-12-myristate-13- acetate Cancer Research 1985 45 10 4955 4962 (Pubitemid 16236179)
28. Matsushima K., Shiroo M., Kung H. F., Copeland T. D., Purification and characterization of a cytosolic 65-kilodalton phosphoprotein in human leukocytes whose phosphorylation is augmented by stimulation with interleukin 1 Biochemistry 1988 27 10 3765 3770
29. Jones S. L., Wang J., Turck C. W., Brown E. J., A role for the actin-bundling protein L-plastin in the regulation of leukocyte integrin function Proceedings of the National Academy of Sciences of the United States of America 1998 95 16 9331 9336 (Pubitemid 28506231)
30. Boldt K., Rist W., Weiss S. M., Weith A., Lenter M. C., FPRL-1 induces modifications of migration-associated proteins in human neutrophils Proteomics 2006 6 17 4790 4799 (Pubitemid 44369058)
31. Hagi A., Hirata H., Shinomiya H., Analysis of a bacterial lipopolysaccharide-activated serine kinase that phosphorylates p65/L-plastin in macrophages Microbiology and Immunology 2006 50 4 331 335 (Pubitemid 46277499)
32. Janji B., Giganti A., de Corte V., Catillon M., Bruyneel E., Lentz D., Plastino J., Gettemans J., Friederich E., Phosphorylation on Ser5 increases the F-actin-binding activity of L-plastin and promotes its targeting to sites of actin assembly in cells Journal of Cell Science 2006 119 9 1947 1960 (Pubitemid 43811019)
33. Al Tanoury Z., Schaffner-Reckinger E., Halavatyi A., Hoffmann C., Moes M., Hadzic E., Catillon M., Yatskou M., Friederich E., Quantitative kinetic study of the actin-bundling protein L-plastin and of its impact on actin turn-over PloS one 2010 5 2 e9210
34. Namba Y., Ito M., Zu Y., Shigesada K., Maruyama K., Human T cell L-plastin bundles actin filaments in a calcium dependent manner Journal of Biochemistry 1992 112 4 503 507
35. Ohsawa K., Imai Y., Sasaki Y., Kohsaka S., Microglia/macrophage-specific protein Iba1 binds to fimbrin and enhances its actin-bundling activity Journal of Neurochemistry 2004 88 4 844 856 (Pubitemid 38199305)
36. Liu F., Shinomiya H., Kirikae T., Hirata H., Asano Y., Characterization of murine grancalcin specifically expressed in leukocytes and its possible role in host defense against bacterial infection Bioscience, Biotechnology and Biochemistry 2004 68 4 894 902 (Pubitemid 39251461)
37. Correia I., Chu D., Chou Y. H., Goldman R. D., Matsudaira P., Integrating the actin and vimentin cytoskeletons: adhesion-dependent formation of fimbrin-vimentin complexes in macrophages The Journal of Cell Biology 1999 146 4 831 842 (Pubitemid 29408908)
38. Wabnitz G. H., Lohneis P., Kirchgessner H., Jahraus B., Gottwald S., Konstandin M., Klemke M., Samstag Y., Sustained LFA-1 cluster formation in the immune synapse requires the combined activities of L-plastin and calmodulin European Journal of Immunology 2010 40 9 2437 2449
39. Paclet M. H., Davis C., Kotsonis P., Godovac-Zimmermann J., Segal A. W., Dekker L. V., N-Formyl peptide receptor subtypes in human neutrophils activate L-plastin phosphorylation through different signal transduction intermediates The Biochemical Journal 2004 377 2 469 477 (Pubitemid 38142202)
40. Borregaard N., Neutrophils, from marrow to microbes Immunity 2010 33 5 657 670
41. Luo B. H., Carman C. V., Springer T. A., Structural basis of integrin regulation and signaling Annual Review of Immunology 2007 25 619 647 (Pubitemid 46697919)
42. Zarbock A., Ley K., Neutrophil adhesion and activation under flow Microcirculation 2009 16 1 31 42
43. Kamen L. A., Schlessinger J., Lowell C. A., Pyk2 is required for neutrophil degranulation and host defense responses to bacterial infection Journal of Immunology 2011 186 3 1656 1665
44. Chen H., Mocsai A., Zhang H., Ding R. X., Morisaki J. H., White M., Rothfork J. M., Heiser P., Colucci-Guyon E., Lowell C. A., Gresham H. D., Allen P. M., Brown E. J., Role for plastin in host defense distinguishes integrin signaling from cell adhesion and spreading Immunity 2003 19 1 95 104 (Pubitemid 36859904)
45. Shibata M., Ohoka T., Mizuno S., Suzuki K., Characterization of a 64-kd protein phosphorylated during chemotactic activation with IL-8 and fMLP of human polymorphonuclear leukocytes. I. Phosphorylation of a 64-kd protein and other proteins Journal of Leukocyte Biology 1993 54 1 1 9 (Pubitemid 23274615)
46. Shibata M., Yamakawa Y., Ohoka T., Mizuno S., Suzuki K., Characterization of a 64-kd protein phosphorylated during chemotactic activation with IL-8 and fMLP of human polymorphonuclear leukocytes. II. Purification and amino acid analysis of phosphorylated 64-kd protein Journal of Leukocyte Biology 1993 54 1 10 16 (Pubitemid 23274616)
47. Rosales C., Jones S. L., McCourt D., Brown E. J., Bromophenacyl bromide binding to the actin-bundling protein l-plastin inhibits inositol trisphosphate-independent increase in Ca 2+ in human neutrophils Proceedings of the National Academy of Sciences of the United States of America 1994 91 9 3534 3538
48. Jones S. L., Brown E. J., FcgammaRII-mediated adhesion and phagocytosis induce L-plastin phosphorylation in human neutrophils The Journal of Biological Chemistry 1996 271 24 14623 14630 (Pubitemid 26190370)
49. Wang J., Brown E. J., Immune complex-induced integrin activation and L-plastin phosphorylation require protein kinase A The Journal of Biological Chemistry 1999 274 34 24349 24356
50. Wang J., Chen H., Brown E. J., L-plastin peptide activation of v 3-mediated adhesion requires integrin conformational change and actin filament disassembly The Journal of Biological Chemistry 2001 276 17 14474 14481
51. Oshizawa T., Yamaguchi T., Suzuki K., Yamamoto Y., Hayakawa T., Possible involvement of optimally phosphorylated L-plastin in activation of superoxide-generating NADPH oxidase Journal of Biochemistry 2003 134 6 827 834 (Pubitemid 38248357)
52. Henning S. W., Meuer S. C., Samstag Y., Serine phosphorylation of a 67-kDa protein in human T lymphocytes represents an accessory receptor-mediated signaling event Journal of Immunology 1994 152 10 4808 4815 (Pubitemid 24139073)
53. Grimbert P., Valanciute A., Audard V., Pawlak A., le gouvelo S., Lang P., Niaudet P., Bensman A., Guellan G., Sahali D., Truncation of C-mip (Tc-mip), a new proximal signaling protein, induces c-maf Th2 transcription factor and cytoskeleton reorganization The Journal of Experimental Medicine 2003 198 5 797 807 (Pubitemid 37087778)
54. Sester U., Wabnitz G. H., Kirchgessner H., Samstag Y., Ras/PI3Kinase/cofilin-independent activation of human CD45RA+ and CD45RO+ T cells by superagonistic CD28 stimulation European Journal of Immunology 2007 37 10 2881 2891 (Pubitemid 47578307)
55. Wabnitz G. H., Kcher T., Lohneis P., Stober C., Konstandin M. H., Funk B., Sester U., Wilm M., Klemke M., Samstag Y., Costimulation induced phosphorylation of L-plastin facilitates surface transport of the T cell activation molecules CD69 and CD25 European Journal of Immunology 2007 37 3 649 662 (Pubitemid 46916932)
56. Chen W., Morley S. C., Donermeyer D., Peng I., Lee W. P., Devoss J., Danilenko D. M., Zhonghua L., Juan Z., Jie Z., Allen P. M., Brown E. J., Actin-bundling protein L-plastin regulates T cell activation Journal of Immunology 2010 185 12 7487 7497
57. Monks C. R., Freiberg B. A., Kupfer H., Sciaky N., Kupfer A., Three-dimensional segregation of supramolecular activation clusters in T cells Nature 1998 395 6697 82 86 (Pubitemid 28420234)
58. Grakoui A., Bromley S. K., Sumen C., Davis M. M., Shaw A. S., Allen P. M., Dustin M. L., The immunological synapse: a molecular machine controlling T cell activation Science 1999 285 5425 221 227 (Pubitemid 29329988)
59. Dustin M. L., Chakraborty A. K., Shaw A. S., Understanding the structure and function of the immunological synapse Cold Spring Harbor Perspectives in Biology 2010 2 10 a002311
60. Pazdrak K., Young T. W., Straub C., Stafford S., Kurosky A., Priming of eosinophils by GM-CSF is mediated by protein kinase CbetaII-phosphorylated L-plastin Journal of Immunology 2011 186 11 6485 6496
61. Wabnitz G. H., Michalke F., Stober C., L-plastin phosphorylation: a novel target for the immunosuppressive drug dexamethasone in primary human T-cells European Journal of Immunology 2011 41 11 3157 3169
62. Batista F. D., Treanor B., Harwood N. E., Visualizing a role for the actin cytoskeleton in the regulation of B-cell activation Immunological Reviews 2010 237 1 191 204
63. Snchez-Madrid F., del Pozo M. A., Leukocyte polarization in cell migration and immune interactions EMBO Journal 1999 18 3 501 511 (Pubitemid 29057235)
64. Friedman R. S., Jacobelli J., Krummel M. F., Mechanisms of T cell motility and arrest: deciphering the relationship between intra- and extracellular determinants Seminars in Immunology 2005 17 6 387 399 (Pubitemid 41654691)
65. Okada T., Cyster J. G., B cell migration and interactions in the early phase of antibody responses Current Opinion in Immunology 2006 18 3 278 285
66. Worbs T., Bernhardt G., Frster R., Factors governing the intranodal migration behavior of T lymphocytes Immunological Reviews 2008 221 1 44 63 (Pubitemid 351230107)
67. Lin S. L., Chien C. W., Han C. L., Chen E. S. W., Kao S. H., Chen Y. J., Liao F., Temporal proteomics profiling of lipid rafts in CCR6-activated T cells reveals the integration of actin cytoskeleton dynamics Journal of Proteome Research 2010 9 1 283 297
68. Morley S. C., Wang C., Lo W. L., Lio C. W. J., Zinselmeyer B. H., Miller M. J., Brown E. J., Allen P. M., The actin-bundling protein L-plastin dissociates CCR7 proximal signaling from CCR7-induced motility Journal of Immunology 2010 184 7 3628 3638
69. Lunn C. A., Reich E. P., Fine J. S., Lavey B., Kozlowski J. A., Hipkin R. W., Lundell D. J., Bober L., Biology and therapeutic potential of cannabinoid CB2 receptor inverse agonists British Journal of Pharmacology 2008 153 2 226 239
70. Todd E. M., Deady L. E., Morley S. C., The actin-bundling protein L-plastin is essential for marginal zone B cell development Journal of Immunology 2011 187 6 3015 3025
71. Edwards J. R., Mundy G. R., Advances in osteoclast biology: old findings and new insights from mouse models Nature Reviews Rheumatology 2011 7 4 235 243
72. Babb S. G., Matsudaira P., Sato M., Correia I., Lim S. S., Fimbrin in podosomes of monocyte-derived osteoclasts Cell Motility and the Cytoskeleton 1997 37 4 308 325 (Pubitemid 27327563)
73. Ma T., Sadashivaiah K., Chellaiah M. A., Regulation of sealing ring formation by L-plastin and cortactin in osteoclasts Journal of Biological Chemistry 2010 285 39 29911 29924
74. Shinomiya H., Hagi A., Fukuzumi M., Mizobuchi M., Hirata H., Utsumi S., Complete primary structure and phosphorylation site of the 65-kDa macrophage protein phosphorylated by stimulation with bacterial lipopolysaccharide Journal of Immunology 1995 154 7 3471 3478
75. Messier J. M., Shaw L. M., Chafel M., Matsudaira P., Mercurio A. M., Fimbrin localized to an insoluble cytoskeletal fraction is constitutively phosphorylated on its headpiece domain in adherent macrophages Cell Motility and the Cytoskeleton 1993 25 3 223 233 (Pubitemid 23198869)
76. Mathias J. R., Dodd M. E., Walters K. B., Yoo S. K., Ranheim E. A., Huttenlocher A., Characterization of zebrafish larval inflammatory macrophages Developmental and Comparative Immunology 2009 33 11 1212 1217
77. Evans J. G., Correia I., Krasavina O., Watson N., Matsudaira P., Macrophage podosomes assemble at the leading lamella by growth and fragmentation The Journal of Cell Biology 2003 161 4 697 705 (Pubitemid 36648753)
78. Lollike K., Johnsen A. H., Durussel I., Borregaard N., Cox J. A., Biochemical characterization of the penta-EF-hand protein grancalcin and identification of L-plastin as a binding partner The Journal of Biological Chemistry 2001 276 21 17762 17769
79. Roes J., Choi B. K., Power D., Xu P., Segal A. W., Granulocyte function in grancalcin-deficient mice Molecular and Cellular Biology 2003 23 3 826 830 (Pubitemid 36133501)
80. Samstag Y., Klemke M., Ectopic expression of L-plastin in human tumor cells: diagnostic and therapeutic implications Advances in Enzyme Regulation 2007 47 118 126 (Pubitemid 47302064)
81. Otsuka M., Kato M., Yoshikawa T., Chen H., Brown E. J., Masuho Y., Omata M., Seki N., Differential expression of the L-plastin gene in human colorectal cancer progression and metastasis Biochemical and Biophysical Research Communications 2001 289 4 876 881 (Pubitemid 34060086)
82. Foran E., McWilliam P., Kelleher D., Croke D. T., Long A., The leukocyte protein L-plastin induces proliferation, invasion and loss of E-cadherin expression in colon cancer cells International Journal of Cancer 2006 118 8 2098 2104
83. Lapillonne A., Coue O., Friederich E., Nicolas A., del Maestro L., Louvard D., Robine S., Sastre-Garu X., Expression patterns of L-plastin isoform in normal and carcinomatous breast tissues Anticancer Research 2000 20 5 3177 3182
84. Janji B., Vallar L., Tanoury Z. A., Bernardin F., Vetter G., Schaffner-Reckinger E., Berchem G., Friederich E., Chouaib S., The actin filament cross-linker L-plastin confers resistance to TNF- in MCF-7 breast cancer cells in a phosphorylation-dependent manner Journal of Cellular and Molecular Medicine 2010 14 6 1264 1275
85. Klemke M., Rafael M. T., Wabnitz G. H., Weschenfelder T., Konstandin M. H., Garbi N., Autschbach F., Hartschuh W., Samstag Y., Phosphorylation of ectopically expressed L-plastin enhances invasiveness of human melanoma cells International Journal of Cancer 2007 120 12 2590 2599 (Pubitemid 46651279)
86. Delanote V., Vanloo B., Catillon M., Friederich E., Vandekerckhove J., Gettemans J., An alpaca single-domain antibody blocks filopodia formation by obstructing L-plastin-mediated F-actin bundling FASEB Journal 2010 24 1 105 118
87. Entschladen F., Gunzer M., Scheuffele C. M., Niggemann B., Znker K. S., T lymphocytes and neutrophil granulocytes differ in regulatory signaling and migratory dynamics with regard to spontaneous locomotion and chemotaxis Cellular Immunology 2000 199 2 104 114 (Pubitemid 30151749)
88. Langereis R J. D., Prinsen B. H. C. M. T., de Sain-van der Velden M. G. M., Coppens C. J. C., Koenderman L., Ulfman L. H., A 2D-DIGE approach to identify proteins involved in inside-out control of integrins Journal of Proteome Research 2009 8 8 3824 3833
89. Shiow L. R., Roadcap D. W., Paris K., Watson S. R., Grigorova I. L., Lebet T., An J., Xu Y., Jenne C. N., Fger N., Sorensen R. U., Goodnow C. C., Bear J. E., Puck J. M., Cyster J. G., The actin regulator coronin 1A is mutant in a thymic egress-deficient mouse strain and in a patient with severe combined immunodeficiency Nature Immunology 2008 9 11 1307 1315
90. Routes J. M., Grossman W. J., Verbsky J., Laessig R. H., Hoffman G. L., Brokopp C. D., Baker M. W., Statewide newborn screening for severe T-cell lymphopenia Journal of the American Medical Association 2009 302 22 2465 2470
91. Engelhardt K. R., McGhee S., Winkler S., Sassi A., Woellner C., Lopez-Herrera G., Chen A., Kim H. S., Lloret M. G., Schulze I., Ehl S., Thiel J., Pfeifer D., Veelken H., Niehues T., Siepermann K., Weinspach S., Reisli I., Keles S., Genel F., Kutuculer N., Camciolu Y., Somer A., Karakoc-Aydiner E., Barlan I., Gennery A., Metin A., Degerliyurt A., Pietrogrande M. C., Yeganeh M., Baz Z., Al-Tamemi S., Klein C., Puck J. M., Holland S. M., McCabe E. R.B., Grimbacher B., Chatila T. A., Large deletions and point mutations involving the dedicator of cytokinesis 8 (DOCK8) in the autosomal-recessive form of hyper-IgE syndrome The Journal of Allergy and Clinical Immunology 2009 124 6 1289 1302.e4
92. Albert M. H., Notarangelo L. D., Ochs H. D., Clinical spectrum, pathophysiology and treatment of the Wiskott-Aldrich syndrome Current Opinion in Hematology 2011 18 1 42 48