Substance P recognition by a subset of human T lymphocytes (original) (raw)

Abstract

The interaction of substance P with human blood T-lymphocytes, which stimulates T-lymphocyte proliferation, was quantified by both flow cytometric and direct binding assays. Fluorescence-detection flow cytometry recorded the binding of dichlorotriazinylamino-fluorescein-labeled substance P to 21 +/- 10% (mean +/- SD, n = 6) and 35 +/- 8% (n = 2) of human blood T-lymphocytes before and after stimulation with 10 micrograms/ml of phytohemagglutinin, respectively. The suppressor-cytotoxic (leu 2a) and helper-inducer (leu 3a) subsets identified by phycoerythrin-labeled monoclonal antibodies contained substance P-reactive T-lymphocytes at respective mean frequencies of 10 and 18%. [3H]substance P bound rapidly and reversibly to a mean of 7035 +/- 2850 sites/T-lymphocyte, which exhibited a dissociation constant (KD) of 1.85 +/- 0.70 X 10(-7) M (mean +/- SD, n = 5). [D-Pro2,D-Phe7,D-Trp9]substance P inhibited the binding of dichlorotriazinylamino-fluorescein-labeled substance P and [3H]substance P to T-lymphocytes at concentrations that suppressed the proliferative response to substance P. Substance P, eledoisin, and substance K (alpha-neurokinin), which all share with substance P the carboxy-terminal substituent -Gly-Leu-Met-NH2, were more potent than substance P in inhibiting the binding of [3H]substance P to T-lymphocytes, suggesting the importance of this sequence in the interaction. Purified human blood B-lymphocytes, monocytes, polymorphonuclear leukocytes, and platelets, and cultured Hut 78 cutaneous lymphoma T-cells, Jurkat cells, Molt-4 lymphoblasts, and HL-60 and U-937 monocyte-like cells all showed only minimal specific binding of [3H]substance P. The recognition of substance P by T-lymphocytes provides one mechanism for selective modulation of immunity by sensory nerves.

1532

Images in this article

Selected References

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

  1. Bar-Shavit Z., Goldman R., Stabinsky Y., Gottlieb P., Fridkin M., Teichberg V. I., Blumberg S. Enhancement of phagocytosis - a newly found activity of substance P residing in its N-terminal tetrapeptide sequence. Biochem Biophys Res Commun. 1980 Jun 30;94(4):1445–1451. doi: 10.1016/0006-291x(80)90581-1. [DOI] [PubMed] [Google Scholar]
  2. Bar-Shavit Z., Teitelbaum S. L., Reitsma P., Hall A., Pegg L. E., Trial J., Kahn A. J. Induction of monocytic differentiation and bone resorption by 1,25-dihydroxyvitamin D3. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5907–5911. doi: 10.1073/pnas.80.19.5907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beed E. A., O'Dorisio M. S., O'Dorisio T. M., Gaginella T. S. Demonstration of a functional receptor for vasoactive intestinal polypeptide on Molt 4b T lymphoblasts. Regul Pept. 1983 Apr;6(1):1–12. doi: 10.1016/0167-0115(83)90129-5. [DOI] [PubMed] [Google Scholar]
  4. Costa M., Furness J. B., Franco R., Llewellyn-Smith I., Murphy R., Beardsley A. M. Substance P in nerve tissue in the gut. Ciba Found Symp. 1982;(91):129–144. doi: 10.1002/9780470720738.ch8. [DOI] [PubMed] [Google Scholar]
  5. Cuello A. C., Kanazawa I. The distribution of substance P immunoreactive fibers in the rat central nervous system. J Comp Neurol. 1978 Mar 1;178(1):129–156. doi: 10.1002/cne.901780108. [DOI] [PubMed] [Google Scholar]
  6. Danek A., O'Dorisio M. S., O'Dorisio T. M., George J. M. Specific binding sites for vasoactive intestinal polypeptide on nonadherent peripheral blood lymphocytes. J Immunol. 1983 Sep;131(3):1173–1177. [PubMed] [Google Scholar]
  7. Gilman S. C., Schwartz J. M., Milner R. J., Bloom F. E., Feldman J. D. beta-Endorphin enhances lymphocyte proliferative responses. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4226–4230. doi: 10.1073/pnas.79.13.4226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goldman D. W., Goetzl E. J. Specific binding of leukotriene B4 to receptors on human polymorphonuclear leukocytes. J Immunol. 1982 Oct;129(4):1600–1604. [PubMed] [Google Scholar]
  9. Hartung H. P., Toyka K. V. Activation of macrophages by substance P: induction of oxidative burst and thromboxane release. Eur J Pharmacol. 1983 May 6;89(3-4):301–305. doi: 10.1016/0014-2999(83)90511-3. [DOI] [PubMed] [Google Scholar]
  10. Hinterberger W., Cerny C., Kinast H., Pointner H., Tragl K. H. Somatostatin reduces the release of colony-stimulating activity (CSA) from PHA-activated mouse spleen lymphocytes. Experientia. 1978 Jul 15;34(7):860–862. doi: 10.1007/BF01939667. [DOI] [PubMed] [Google Scholar]
  11. Hökfelt T., Kellerth J. O., Nilsson G., Pernow B. Substance p: localization in the central nervous system and in some primary sensory neurons. Science. 1975 Nov 28;190(4217):889–890. doi: 10.1126/science.242075. [DOI] [PubMed] [Google Scholar]
  12. Johnson A. R., Erdös E. G. Release of histamine from mast cells by vasoactive peptides. Proc Soc Exp Biol Med. 1973 Apr;142(4):1252–1256. doi: 10.3181/00379727-142-37219. [DOI] [PubMed] [Google Scholar]
  13. Johnson H. M., Smith E. M., Torres B. A., Blalock J. E. Regulation of the in vitro antibody response by neuroendocrine hormones. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4171–4174. doi: 10.1073/pnas.79.13.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ljungdahl A., Hökfelt T., Nilsson G., Goldstein M. Distribution of substance P-like immunoreactivity in the central nervous system of the rat--II. Light microscopic localization in relation to catecholamine-containing neurons. Neuroscience. 1978;3(10):945–976. doi: 10.1016/0306-4522(78)90117-3. [DOI] [PubMed] [Google Scholar]
  15. Mangelsdorf D. J., Koeffler H. P., Donaldson C. A., Pike J. W., Haussler M. R. 1,25-Dihydroxyvitamin D3-induced differentiation in a human promyelocytic leukemia cell line (HL-60): receptor-mediated maturation to macrophage-like cells. J Cell Biol. 1984 Feb;98(2):391–398. doi: 10.1083/jcb.98.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mathews P. M., Froelich C. J., Sibbitt W. L., Jr, Bankhurst A. D. Enhancement of natural cytotoxicity by beta-endorphin. J Immunol. 1983 Apr;130(4):1658–1662. [PubMed] [Google Scholar]
  17. Murakoshi T., Yanagisawa M., Kitada C., Fujino M., Otsuka M. The role of the N-terminus in the active conformation of the substance P analogues. Eur J Pharmacol. 1983 May 20;90(1):133–137. doi: 10.1016/0014-2999(83)90225-x. [DOI] [PubMed] [Google Scholar]
  18. Nawa H., Hirose T., Takashima H., Inayama S., Nakanishi S. Nucleotide sequences of cloned cDNAs for two types of bovine brain substance P precursor. Nature. 1983 Nov 3;306(5938):32–36. doi: 10.1038/306032a0. [DOI] [PubMed] [Google Scholar]
  19. Payan D. G., Brewster D. R., Goetzl E. J. Specific stimulation of human T lymphocytes by substance P. J Immunol. 1983 Oct;131(4):1613–1615. [PubMed] [Google Scholar]
  20. Payan D. G., Goetzl E. J. Specific suppression of human T lymphocyte function by leukotriene B4. J Immunol. 1983 Aug;131(2):551–553. [PubMed] [Google Scholar]
  21. Payan D. G., Hess C. A., Goetzl E. J. Inhibition by somatostatin of the proliferation of T-lymphocytes and Molt-4 lymphoblasts. Cell Immunol. 1984 Apr 1;84(2):433–438. doi: 10.1016/0008-8749(84)90117-5. [DOI] [PubMed] [Google Scholar]
  22. Payan D. G., Missirian-Bastian A., Goetzl E. J. Human T-lymphocyte subset specificity of the regulatory effects of leukotriene B4. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3501–3505. doi: 10.1073/pnas.81.11.3501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Payan D. G., Trentham D. E., Goetzl E. J. Modulation of human lymphocyte function by C3a and C3a(70-77). J Exp Med. 1982 Sep 1;156(3):756–765. doi: 10.1084/jem.156.3.756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pernow B. Substance P. Pharmacol Rev. 1983 Jun;35(2):85–141. [PubMed] [Google Scholar]
  25. Valone F. H., Coles E., Reinhold V. R., Goetzl E. J. Specific binding of phospholipid platelet-activating factor by human platelets. J Immunol. 1982 Oct;129(4):1637–1641. [PubMed] [Google Scholar]
  26. Watt K. W., Brightman I. L., Goetzl E. J. Isolation of two polypeptides comprising the neutrophil-immobilizing factor of human leucocytes. Immunology. 1983 Jan;48(1):79–86. [PMC free article] [PubMed] [Google Scholar]
  27. Wybran J., Appelboom T., Famaey J. P., Govaerts A. Suggestive evidence for receptors for morphine and methionine-enkephalin on normal human blood T lymphocytes. J Immunol. 1979 Sep;123(3):1068–1070. [PubMed] [Google Scholar]