Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1998 Mar 15;330(Pt 3):1129–1135. doi: 10.1042/bj3301129

CD38 binding to human myeloid cells is mediated by mouse and human CD31.

A L Horenstein 1, H Stockinger 1, B A Imhof 1, F Malavasi 1
PMCID: PMC1219253  PMID: 9494077

Abstract

Soluble forms of membrane receptors are emerging candidates as physiological regulators of leukocyte trafficking. In the present study, we found that the soluble form of the CD38 antigen (sCD38) bears a binding domain of low affinity for a cellular receptor on U937 cells. Cross-linking and peptide-mapping studies confirmed the physical association and the identification of the U937 receptor as a 130 kDa protein. The binding of sCD38 to the receptor was differentially inhibited by several monoclonal antibodies against the CD31 cell-adhesion molecule. Thus the interaction was analysed through direct association of soluble and membrane CD38 with soluble recombinant murine CD31 with three N-terminal and with all six extracellular Ig domains. Cross-linking experiments on U937 intact cells, and ligand blot assays of the immunoprecipitated CD38 molecule, indicated that (i) the recognized epitope is determined by the tertiary structure of the molecule, and that (ii) the binding domain involved resides in the ectocellular portion of the CD31 molecule, more precisely in the first three N-terminal domains. A comparative functional activity between murine and human CD31 was also explored. The data presented suggest that (i) human CD31 bears a highly functional similarity with its murine counterpart, as it is a receptor in myeloid cells with more than one ligand (the alphavbeta3 integrin and the CD38 molecule), and that (ii) the activity of sCD38 as decoy molecule for CD31 may play an important role in cell-cell interactions in physiological and pathological conditions.

Full Text

The Full Text of this article is available as a PDF (329.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Belli S. I., Sali A., Goding J. W. Divalent cations stabilize the conformation of plasma cell membrane glycoprotein PC-1 (alkaline phosphodiesterase I). Biochem J. 1994 Nov 15;304(Pt 1):75–80. doi: 10.1042/bj3040075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bogen S., Pak J., Garifallou M., Deng X., Muller W. A. Monoclonal antibody to murine PECAM-1 (CD31) blocks acute inflammation in vivo. J Exp Med. 1994 Mar 1;179(3):1059–1064. doi: 10.1084/jem.179.3.1059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buckley C. D., Doyonnas R., Newton J. P., Blystone S. D., Brown E. J., Watt S. M., Simmons D. L. Identification of alpha v beta 3 as a heterotypic ligand for CD31/PECAM-1. J Cell Sci. 1996 Feb;109(Pt 2):437–445. doi: 10.1242/jcs.109.2.437. [DOI] [PubMed] [Google Scholar]
  4. Cartwright J. E., Whitley G. S., Johnstone A. P. The expression and release of adhesion molecules by human endothelial cell lines and their consequent binding of lymphocytes. Exp Cell Res. 1995 Apr;217(2):329–335. doi: 10.1006/excr.1995.1094. [DOI] [PubMed] [Google Scholar]
  5. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  6. Colotta F., Dower S. K., Sims J. E., Mantovani A. The type II 'decoy' receptor: a novel regulatory pathway for interleukin 1. Immunol Today. 1994 Dec;15(12):562–566. doi: 10.1016/0167-5699(94)90217-8. [DOI] [PubMed] [Google Scholar]
  7. DeLisser H. M., Newman P. J., Albelda S. M. Molecular and functional aspects of PECAM-1/CD31. Immunol Today. 1994 Oct;15(10):490–495. doi: 10.1016/0167-5699(94)90195-3. [DOI] [PubMed] [Google Scholar]
  8. DeLisser H. M., Yan H. C., Newman P. J., Muller W. A., Buck C. A., Albelda S. M. Platelet/endothelial cell adhesion molecule-1 (CD31)-mediated cellular aggregation involves cell surface glycosaminoglycans. J Biol Chem. 1993 Jul 25;268(21):16037–16046. [PubMed] [Google Scholar]
  9. Deaglio S., Dianzani U., Horenstein A. L., Fernández J. E., van Kooten C., Bragardo M., Funaro A., Garbarino G., Di Virgilio F., Banchereau J. Human CD38 ligand. A 120-KDA protein predominantly expressed on endothelial cells. J Immunol. 1996 Jan 15;156(2):727–734. [PubMed] [Google Scholar]
  10. Dianzani U., Funaro A., DiFranco D., Garbarino G., Bragardo M., Redoglia V., Buonfiglio D., De Monte L. B., Pileri A., Malavasi F. Interaction between endothelium and CD4+CD45RA+ lymphocytes. Role of the human CD38 molecule. J Immunol. 1994 Aug 1;153(3):952–959. [PubMed] [Google Scholar]
  11. Drach J., McQueen T., Engel H., Andreeff M., Robertson K. A., Collins S. J., Malavasi F., Mehta K. Retinoic acid-induced expression of CD38 antigen in myeloid cells is mediated through retinoic acid receptor-alpha. Cancer Res. 1994 Apr 1;54(7):1746–1752. [PubMed] [Google Scholar]
  12. Fawcett J., Buckley C., Holness C. L., Bird I. N., Spragg J. H., Saunders J., Harris A., Simmons D. L. Mapping the homotypic binding sites in CD31 and the role of CD31 adhesion in the formation of interendothelial cell contacts. J Cell Biol. 1995 Mar;128(6):1229–1241. doi: 10.1083/jcb.128.6.1229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Funaro A., De Monte L. B., Dianzani U., Forni M., Malavasi F. Human CD38 is associated to distinct molecules which mediate transmembrane signaling in different lineages. Eur J Immunol. 1993 Oct;23(10):2407–2411. doi: 10.1002/eji.1830231005. [DOI] [PubMed] [Google Scholar]
  14. Funaro A., Horenstein A. L., Calosso L., Morra M., Tarocco R. P., Franco L., De Flora A., Malavasi F. Identification and characterization of an active soluble form of human CD38 in normal and pathological fluids. Int Immunol. 1996 Nov;8(11):1643–1650. doi: 10.1093/intimm/8.11.1643. [DOI] [PubMed] [Google Scholar]
  15. Funaro A., Spagnoli G. C., Ausiello C. M., Alessio M., Roggero S., Delia D., Zaccolo M., Malavasi F. Involvement of the multilineage CD38 molecule in a unique pathway of cell activation and proliferation. J Immunol. 1990 Oct 15;145(8):2390–2396. [PubMed] [Google Scholar]
  16. Gearing A. J., Newman W. Circulating adhesion molecules in disease. Immunol Today. 1993 Oct;14(10):506–512. doi: 10.1016/0167-5699(93)90267-O. [DOI] [PubMed] [Google Scholar]
  17. Graeff R. M., Walseth T. F., Fryxell K., Branton W. D., Lee H. C. Enzymatic synthesis and characterizations of cyclic GDP-ribose. A procedure for distinguishing enzymes with ADP-ribosyl cyclase activity. J Biol Chem. 1994 Dec 2;269(48):30260–30267. [PubMed] [Google Scholar]
  18. Howard M., Grimaldi J. C., Bazan J. F., Lund F. E., Santos-Argumedo L., Parkhouse R. M., Walseth T. F., Lee H. C. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science. 1993 Nov 12;262(5136):1056–1059. doi: 10.1126/science.8235624. [DOI] [PubMed] [Google Scholar]
  19. Imhof B. A., Dunon D. Leukocyte migration and adhesion. Adv Immunol. 1995;58:345–416. doi: 10.1016/s0065-2776(08)60623-9. [DOI] [PubMed] [Google Scholar]
  20. Kontani K., Kukimoto I., Nishina H., Hoshino S., Hazeki O., Kanaho Y., Katada T. Tyrosine phosphorylation of the c-cbl proto-oncogene product mediated by cell surface antigen CD38 in HL-60 cells. J Biol Chem. 1996 Jan 19;271(3):1534–1537. doi: 10.1074/jbc.271.3.1534. [DOI] [PubMed] [Google Scholar]
  21. Kontani K., Nishina H., Ohoka Y., Takahashi K., Katada T. NAD glycohydrolase specifically induced by retinoic acid in human leukemic HL-60 cells. Identification of the NAD glycohydrolase as leukocyte cell surface antigen CD38. J Biol Chem. 1993 Aug 15;268(23):16895–16898. [PubMed] [Google Scholar]
  22. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Malavasi F., Funaro A., Roggero S., Horenstein A., Calosso L., Mehta K. Human CD38: a glycoprotein in search of a function. Immunol Today. 1994 Mar;15(3):95–97. doi: 10.1016/0167-5699(94)90148-1. [DOI] [PubMed] [Google Scholar]
  24. Mariani M., Bracci L., Presentini R., Nucci D., Neri P., Antoni G. Immunogenicity of a free synthetic peptide: carrier-conjugation enhances antibody affinity for the native protein. Mol Immunol. 1987 Mar;24(3):297–303. doi: 10.1016/0161-5890(87)90148-9. [DOI] [PubMed] [Google Scholar]
  25. Muller W. A., Berman M. E., Newman P. J., DeLisser H. M., Albelda S. M. A heterophilic adhesion mechanism for platelet/endothelial cell adhesion molecule 1 (CD31). J Exp Med. 1992 May 1;175(5):1401–1404. doi: 10.1084/jem.175.5.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Newman P. J., Berndt M. C., Gorski J., White G. C., 2nd, Lyman S., Paddock C., Muller W. A. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science. 1990 Mar 9;247(4947):1219–1222. doi: 10.1126/science.1690453. [DOI] [PubMed] [Google Scholar]
  27. Piali L., Hammel P., Uherek C., Bachmann F., Gisler R. H., Dunon D., Imhof B. A. CD31/PECAM-1 is a ligand for alpha v beta 3 integrin involved in adhesion of leukocytes to endothelium. J Cell Biol. 1995 Jul;130(2):451–460. doi: 10.1083/jcb.130.2.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Prager E., Sunder-Plassmann R., Hansmann C., Koch C., Holter W., Knapp W., Stockinger H. Interaction of CD31 with a heterophilic counterreceptor involved in downregulation of human T cell responses. J Exp Med. 1996 Jul 1;184(1):41–50. doi: 10.1084/jem.184.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rhodes B. A., Buckelew J. M., Pant K. D., Hinkle G. H. Quality control test for immunoreactivity of radiolabeled antibody. Biotechniques. 1990 Jan;8(1):70–75. [PubMed] [Google Scholar]
  30. Shimizu Y., Mobley J. L. Distinct divalent cation requirements for integrin-mediated CD4+ T lymphocyte adhesion to ICAM-1, fibronectin, VCAM-1, and invasin. J Immunol. 1993 Oct 15;151(8):4106–4115. [PubMed] [Google Scholar]
  31. Silvennoinen O., Nishigaki H., Kitanaka A., Kumagai M., Ito C., Malavasi F., Lin Q., Conley M. E., Campana D. CD38 signal transduction in human B cell precursors. Rapid induction of tyrosine phosphorylation, activation of syk tyrosine kinase, and phosphorylation of phospholipase C-gamma and phosphatidylinositol 3-kinase. J Immunol. 1996 Jan 1;156(1):100–107. [PubMed] [Google Scholar]
  32. Springer T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994 Jan 28;76(2):301–314. doi: 10.1016/0092-8674(94)90337-9. [DOI] [PubMed] [Google Scholar]
  33. Stockinger H., Gadd S. J., Eher R., Majdic O., Schreiber W., Kasinrerk W., Strass B., Schnabl E., Knapp W. Molecular characterization and functional analysis of the leukocyte surface protein CD31. J Immunol. 1990 Dec 1;145(11):3889–3897. [PubMed] [Google Scholar]
  34. Stoolman L. M., Kaldjian E. Adhesion molecules involved in the trafficking of normal and malignant leukocytes. Invasion Metastasis. 1992;12(2):101–111. [PubMed] [Google Scholar]
  35. Warrell R. P., Jr, de Thé H., Wang Z. Y., Degos L. Acute promyelocytic leukemia. N Engl J Med. 1993 Jul 15;329(3):177–189. doi: 10.1056/NEJM199307153290307. [DOI] [PubMed] [Google Scholar]
  36. Xie Y., Muller W. A. Molecular cloning and adhesive properties of murine platelet/endothelial cell adhesion molecule 1. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5569–5573. doi: 10.1073/pnas.90.12.5569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zocchi E., Franco L., Guida L., Benatti U., Bargellesi A., Malavasi F., Lee H. C., De Flora A. A single protein immunologically identified as CD38 displays NAD+ glycohydrolase, ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase activities at the outer surface of human erythrocytes. Biochem Biophys Res Commun. 1993 Nov 15;196(3):1459–1465. doi: 10.1006/bbrc.1993.2416. [DOI] [PubMed] [Google Scholar]
  38. Zubiaur M., Izquierdo M., Terhorst C., Malavasi F., Sancho J. CD38 ligation results in activation of the Raf-1/mitogen-activated protein kinase and the CD3-zeta/zeta-associated protein-70 signaling pathways in Jurkat T lymphocytes. J Immunol. 1997 Jul 1;159(1):193–205. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES