A mutation in the human tetraspanin CD81 gene is expressed as a truncated protein but does not enable CD19 maturation and cell surface expression

Journal of Clinical Immunology

Volumn 35, Issue 3, 2015, Pages 254-263

  Vences Catalán, Felipe ^a   Kuo, Chiung Chi ^a   Sagi, Yael ^a   Chen, Homer ^a   Kela Madar, Neta ^a   van Zelm, Menno C ^b   van Dongen, Jacques J M ^b   Levy, Shoshana ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

B cells; ER; glycosylation; Protein trafficking

Indexed keywords

CD19 ANTIGEN; CD81 ANTIGEN; CD81 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL SURFACE; CHIMERA; CONTROLLED STUDY; FLOW CYTOMETRY; GENE MUTATION; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INDUCTION, SYNTHESIS AND MODIFICATION; PROTEIN PROCESSING; PROTEIN TRAFFICKING; WESTERN BLOTTING; ANIMAL; CELL LINE; CELL MEMBRANE; GENETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT;

ANIMALS; ANTIGENS, CD19; ANTIGENS, CD81; B-LYMPHOCYTES; CELL LINE; CELL MEMBRANE; HEPATOCYTES; HUMANS; MICE; MUTATION; PROTEIN TRANSPORT;

EID: 84925517323     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-015-0148-2     Document Type: Article

References (32)

1. Shoham T, Rajapaksa R, Boucheix C, Rubinstein E, Poe JC, Tedder TF, et al. The tetraspanin CD81 regulates the expression of CD19 during B cell development in a postendoplasmic reticulum compartment. J Immunol. 2003;171(8):4062–72.
2. Miyazaki T, Muller U, Campbell KS. Normal development but differentially altered proliferative responses of lymphocytes in mice lacking CD81. Embo J. 1997;16(14):4217–25.
3. Tsitsikov EN, Gutierrez-Ramos JC, Geha RS. Impaired CD19 expression and signaling, enhanced antibody response to type II T independent antigen and reduction of B-1 cells in CD81-deficient mice. Proc Natl Acad Sci U S A. 1997;94(20):10844–9.
4. Maecker HT, Levy S. Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J Exp Med. 1997;185(8):1505–10.
5. van Zelm MC, Smet J, Adams B, Mascart F, Schandene L, Janssen F, et al. CD81 gene defect in humans disrupts CD19 complex formation and leads to antibody deficiency. J Clin Invest. 2010;120(4):1265–74.
6. van Zelm MC, Reisli I, van der Burg M, Castano D, van Noesel CJ, van Tol MJ, et al. An antibody-deficiency syndrome due to mutations in the CD19 gene. N Engl J Med. 2006;354(18):1901–12.
7. Kanegane H, Agematsu K, Futatani T, Sira MM, Suga K, Sekiguchi T, et al. Novel mutations in a Japanese patient with CD19 deficiency. Genes Immun. 2007;8(8):663–70.
8. Tedder TF. CD19: a promising B cell target for rheumatoid arthritis. Nat Rev Rheumatol. 2009;5(10):572–7.
9. Sato S, Steeber DA, Jansen PJ, Tedder TF. CD19 expression levels regulate B lymphocyte development: human CD19 restores normal function in mice lacking endogenous CD19. J Immunol. 1997;158(10):4662–9.
10. Bradbury LE, Goldmacher VS, Tedder TF. The CD19 signal transduction complex of B lymphocytes. Deletion of the CD19 cytoplasmic domain alters signal transduction but not complex formation with TAPA-1 and Leu 13. J Immunol. 1993;151(6):2915–27.
11. Bradbury LE, Kansas GS, Levy S, Evans RL, Tedder TF. The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. J Immunol. 1992;149(9):2841–50.
12. Matsumoto AK, Martin DR, Carter RH, Klickstein LB, Ahearn JM, Fearon DT. Functional dissection of the CD21/CD19/TAPA-1/Leu-13 complex of B lymphocytes. J Exp Med. 1993;178(4):1407–17.
13. Fearon DT, Carroll MC. Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu Rev Immunol. 2000;18:393–422.
14. Sato S, Miller AS, Howard MC, Tedder TF. Regulation of B lymphocyte development and activation by the CD19/CD21/CD81/Leu 13 complex requires the cytoplasmic domain of CD19. J Immunol. 1997;159(7):3278–87.
15. Rocha-Perugini V, Lavie M, Delgrange D, Canton J, Pillez A, Potel J, et al. The association of CD81 with tetraspanin-enriched microdomains is not essential for Hepatitis C virus entry. BMC Microbiol. 2009;9:111.
16. Higginbottom A, Quinn ER, Kuo CC, Flint M, Wilson LH, Bianchi E, et al. Identification of amino acid residues in CD81 critical for interaction with hepatitis C virus envelope glycoprotein E2. J Virol. 2000;74(8):3642–9.
17. Shoham T, Rajapaksa R, Kuo CC, Haimovich J, Levy S. Building of the tetraspanin web: distinct structural domains of CD81 function in different cellular compartments. Mol Cell Biol. 2006;26(4):1373–85.
18. Rocha-Perugini V, Zamai M, Gonzalez-Granado JM, Barreiro O, Tejera E, Yanez-Mo M, et al. CD81 controls sustained T cell activation signaling and defines the maturation stages of cognate immunological synapses. Mol Cell Biol. 2013;33(18):3644–58.
19. Harman C, Zhong L, Ma L, Liu P, Deng L, Zhao Z, et al. A View of the E2-CD81 Interface at the Binding Site of a Neutralizing Antibody against Hepatitis C Virus. J Virol. 2015;89(1):492–501.
20. Kitadokoro K, Bordo D, Galli G, Petracca R, Falugi F, Abrignani S, et al. CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. Embo J. 2001;20(1–2):12–8.
21. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006;3(12):995–1000.
22. Levy S, Shoham T. The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol. 2005;5(2):136–48.
23. Engel P, Zhou LJ, Ord DC, Sato S, Koller B, Tedder TF. Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity. 1995;3(1):39–50.
24. Homsi Y, Schloetel JG, Scheffer KD, Schmidt TH, Destainville N, Florin L, et al. The extracellular delta-domain is essential for the formation of CD81 tetraspanin webs. Biophys J. 2014;107(1):100–13.
25. Russ WP, Engelman DM. The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol. 2000;296(3):911–9.
26. Berditchevski F, Odintsova E. Tetraspanins as regulators of protein trafficking. Traffic. 2007;8(2):89–96.
27. Manolios N, Bonifacino JS, Klausner RD. Transmembrane helical interactions and the assembly of the T cell receptor complex. Science. 1990;249(4966):274–7.
28. Fink A, Sal-Man N, Gerber D, Shai Y. Transmembrane domains interactions within the membrane milieu: principles, advances and challenges. Biochim Biophys Acta. 2012;1818(4):974–83.
29. Seigneuret M. Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: conserved and variable structural domains in the tetraspanin superfamily. Biophys J. 2006;90(1):212–27.
30. Dornier E, Coumailleau F, Ottavi JF, Moretti J, Boucheix C, Mauduit P, et al. TspanC8 tetraspanins regulate ADAM10/Kuzbanian trafficking and promote Notch activation in flies and mammals. J Cell Biol. 2012;199(3):481–96.
31. Haining EJ, Yang J, Bailey RL, Khan K, Collier R, Tsai S, et al. The TspanC8 subgroup of tetraspanins interacts with A disintegrin and metalloprotease 10 (ADAM10) and regulates its maturation and cell surface expression. J Biol Chem. 2012;287(47):39753–65.
32. Prox J, Willenbrock M, Weber S, Lehmann T, Schmidt-Arras D, Schwanbeck R, et al. Tetraspanin15 regulates cellular trafficking and activity of the ectodomain sheddase ADAM10. Cell Mol Life Sci. 2012;69(17):2919–32.