Abstract
Murine interleukin-5 (IL-5) is known to play an essential role in Ig production of B cells and proliferation and differentiation of eosinophils. Here, we have isolated cDNA clones encoding a murine IL-5 receptor by expression screening of a library prepared from a murine IL-5 dependent early B cell line. A cDNA library was expressed in COS7 cells and screened by panning with the use of anti-IL-5 receptor monoclonal antibodies. The deduced amino acid sequence analysis demonstrates that the receptor is a glycoprotein of 415 amino acids (Mr 45,284), including an N-terminal hydrophobic region (17 amino acids), a glycosylated extracellular domain (322 amino acids), a single transmembrane segment (22 amino acids) and a cytoplasmic tail (54 amino acids). COS7 cells transfected with the cDNA expressed a 60 kd protein that bound IL-5 with a single class of affinity (KD = 2-10 nM). FDC-P1 cells transfected with the cDNA for murine IL-5 receptor showed the expression of IL-5 binding sites with both low (KD = 6 nM) and high affinity (KD = 30 pM) and acquired responsiveness to IL-5 for proliferation, although parental FDC-P1 cells did not show any detectable IL-5 binding. In addition, several cDNA clones encoding soluble forms of the IL-5 receptor were isolated. Northern blot analysis showed that two species of mRNAs (5.0 kb and 5.8 kb) were detected in cell lines that display binding sites for murine IL-5. Homology search for the amino acid sequence of the IL-5 receptor reveals that the IL-5 receptor contains a common motif of a cytokine receptor family that is recently identified.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Azuma C., Tanabe T., Konishi M., Kinashi T., Noma T., Matsuda F., Yaoita Y., Takatsu K., Hammarström L., Smith C. I. Cloning of cDNA for human T-cell replacing factor (interleukin-5) and comparison with the murine homologue. Nucleic Acids Res. 1986 Nov 25;14(22):9149–9158. doi: 10.1093/nar/14.22.9149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baumbach W. R., Horner D. L., Logan J. S. The growth hormone-binding protein in rat serum is an alternatively spliced form of the rat growth hormone receptor. Genes Dev. 1989 Aug;3(8):1199–1205. doi: 10.1101/gad.3.8.1199. [DOI] [PubMed] [Google Scholar]
- Bazan J. F. A novel family of growth factor receptors: a common binding domain in the growth hormone, prolactin, erythropoietin and IL-6 receptors, and the p75 IL-2 receptor beta-chain. Biochem Biophys Res Commun. 1989 Oct 31;164(2):788–795. doi: 10.1016/0006-291x(89)91528-3. [DOI] [PubMed] [Google Scholar]
- Boutin J. M., Jolicoeur C., Okamura H., Gagnon J., Edery M., Shirota M., Banville D., Dusanter-Fourt I., Djiane J., Kelly P. A. Cloning and expression of the rat prolactin receptor, a member of the growth hormone/prolactin receptor gene family. Cell. 1988 Apr 8;53(1):69–77. doi: 10.1016/0092-8674(88)90488-6. [DOI] [PubMed] [Google Scholar]
- D'Andrea A. D., Fasman G. D., Lodish H. F. Erythropoietin receptor and interleukin-2 receptor beta chain: a new receptor family. Cell. 1989 Sep 22;58(6):1023–1024. doi: 10.1016/0092-8674(89)90499-6. [DOI] [PubMed] [Google Scholar]
- D'Andrea A. D., Lodish H. F., Wong G. G. Expression cloning of the murine erythropoietin receptor. Cell. 1989 Apr 21;57(2):277–285. doi: 10.1016/0092-8674(89)90965-3. [DOI] [PubMed] [Google Scholar]
- Fukunaga R., Ishizaka-Ikeda E., Seto Y., Nagata S. Expression cloning of a receptor for murine granulocyte colony-stimulating factor. Cell. 1990 Apr 20;61(2):341–350. doi: 10.1016/0092-8674(90)90814-u. [DOI] [PubMed] [Google Scholar]
- Gearing D. P., King J. A., Gough N. M., Nicola N. A. Expression cloning of a receptor for human granulocyte-macrophage colony-stimulating factor. EMBO J. 1989 Dec 1;8(12):3667–3676. doi: 10.1002/j.1460-2075.1989.tb08541.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodwin R. G., Friend D., Ziegler S. F., Jerzy R., Falk B. A., Gimpel S., Cosman D., Dower S. K., March C. J., Namen A. E. Cloning of the human and murine interleukin-7 receptors: demonstration of a soluble form and homology to a new receptor superfamily. Cell. 1990 Mar 23;60(6):941–951. doi: 10.1016/0092-8674(90)90342-c. [DOI] [PubMed] [Google Scholar]
- Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
- Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. doi: 10.1126/science.3291115. [DOI] [PubMed] [Google Scholar]
- Harada N., Matsumoto M., Koyama N., Shimizu A., Honjo T., Tominaga A., Takatsu K. T cell replacing factor/interleukin 5 induces not only B-cell growth and differentiation, but also increased expression of interleukin 2 receptor on activated B-cells. Immunol Lett. 1987 Jul;15(3):205–215. doi: 10.1016/0165-2478(87)90026-5. [DOI] [PubMed] [Google Scholar]
- Hatakeyama M., Tsudo M., Minamoto S., Kono T., Doi T., Miyata T., Miyasaka M., Taniguchi T. Interleukin-2 receptor beta chain gene: generation of three receptor forms by cloned human alpha and beta chain cDNA's. Science. 1989 May 5;244(4904):551–556. doi: 10.1126/science.2785715. [DOI] [PubMed] [Google Scholar]
- Hitoshi Y., Yamaguchi N., Mita S., Sonoda E., Takaki S., Tominaga A., Takatsu K. Distribution of IL-5 receptor-positive B cells. Expression of IL-5 receptor on Ly-1(CD5)+ B cells. J Immunol. 1990 Jun 1;144(11):4218–4225. [PubMed] [Google Scholar]
- Itoh N., Yonehara S., Schreurs J., Gorman D. M., Maruyama K., Ishii A., Yahara I., Arai K., Miyajima A. Cloning of an interleukin-3 receptor gene: a member of a distinct receptor gene family. Science. 1990 Jan 19;247(4940):324–327. doi: 10.1126/science.2404337. [DOI] [PubMed] [Google Scholar]
- Kinashi T., Harada N., Severinson E., Tanabe T., Sideras P., Konishi M., Azuma C., Tominaga A., Bergstedt-Lindqvist S., Takahashi M. Cloning of complementary DNA encoding T-cell replacing factor and identity with B-cell growth factor II. Nature. 1986 Nov 6;324(6092):70–73. doi: 10.1038/324070a0. [DOI] [PubMed] [Google Scholar]
- Leung D. W., Spencer S. A., Cachianes G., Hammonds R. G., Collins C., Henzel W. J., Barnard R., Waters M. J., Wood W. I. Growth hormone receptor and serum binding protein: purification, cloning and expression. Nature. 1987 Dec 10;330(6148):537–543. doi: 10.1038/330537a0. [DOI] [PubMed] [Google Scholar]
- Loughnan M. S., Takatsu K., Harada N., Nossal G. J. T-cell-replacing factor (interleukin 5) induces expression of interleukin 2 receptors on murine splenic B cells. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5399–5403. doi: 10.1073/pnas.84.15.5399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mita S., Harada N., Naomi S., Hitoshi Y., Sakamoto K., Akagi M., Tominaga A., Takatsu K. Receptors for T cell-replacing factor/interleukin 5. Specificity, quantitation, and its implication. J Exp Med. 1988 Sep 1;168(3):863–878. doi: 10.1084/jem.168.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mita S., Tominaga A., Hitoshi Y., Sakamoto K., Honjo T., Akagi M., Kikuchi Y., Yamaguchi N., Takatsu K. Characterization of high-affinity receptors for interleukin 5 on interleukin 5-dependent cell lines. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2311–2315. doi: 10.1073/pnas.86.7.2311. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miyazaki J., Takaki S., Araki K., Tashiro F., Tominaga A., Takatsu K., Yamamura K. Expression vector system based on the chicken beta-actin promoter directs efficient production of interleukin-5. Gene. 1989 Jul 15;79(2):269–277. doi: 10.1016/0378-1119(89)90209-6. [DOI] [PubMed] [Google Scholar]
- Mosley B., Beckmann M. P., March C. J., Idzerda R. L., Gimpel S. D., VandenBos T., Friend D., Alpert A., Anderson D., Jackson J. The murine interleukin-4 receptor: molecular cloning and characterization of secreted and membrane bound forms. Cell. 1989 Oct 20;59(2):335–348. doi: 10.1016/0092-8674(89)90295-x. [DOI] [PubMed] [Google Scholar]
- Nakanishi K., Yoshimoto T., Katoh Y., Ono S., Matsui K., Hiroishi K., Noma T., Honjo T., Takatsu K., Higashino K. Both B151-T cell replacing factor 1 and IL-5 regulate Ig secretion and IL-2 receptor expression on a cloned B lymphoma line. J Immunol. 1988 Feb 15;140(4):1168–1174. [PubMed] [Google Scholar]
- Okayama H., Kawaichi M., Brownstein M., Lee F., Yokota T., Arai K. High-efficiency cloning of full-length cDNA; construction and screening of cDNA expression libraries for mammalian cells. Methods Enzymol. 1987;154:3–28. doi: 10.1016/0076-6879(87)54067-8. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seed B. An LFA-3 cDNA encodes a phospholipid-linked membrane protein homologous to its receptor CD2. 1987 Oct 29-Nov 4Nature. 329(6142):840–842. doi: 10.1038/329840a0. [DOI] [PubMed] [Google Scholar]
- Seed B., Aruffo A. Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc Natl Acad Sci U S A. 1987 May;84(10):3365–3369. doi: 10.1073/pnas.84.10.3365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sims J. E., March C. J., Cosman D., Widmer M. B., MacDonald H. R., McMahan C. J., Grubin C. E., Wignall J. M., Jackson J. L., Call S. M. cDNA expression cloning of the IL-1 receptor, a member of the immunoglobulin superfamily. Science. 1988 Jul 29;241(4865):585–589. doi: 10.1126/science.2969618. [DOI] [PubMed] [Google Scholar]
- Snapper C. M., Finkelman F. D., Paul W. E. Regulation of IgG1 and IgE production by interleukin 4. Immunol Rev. 1988 Feb;102:51–75. doi: 10.1111/j.1600-065x.1988.tb00741.x. [DOI] [PubMed] [Google Scholar]
- Sonoda E., Matsumoto R., Hitoshi Y., Ishii T., Sugimoto M., Araki S., Tominaga A., Yamaguchi N., Takatsu K. Transforming growth factor beta induces IgA production and acts additively with interleukin 5 for IgA production. J Exp Med. 1989 Oct 1;170(4):1415–1420. doi: 10.1084/jem.170.4.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swain S. L., Howard M., Kappler J., Marrack P., Watson J., Booth R., Wetzel G. D., Dutton R. W. Evidence for two distinct classes of murine B cell growth factors with activities in different functional assays. J Exp Med. 1983 Sep 1;158(3):822–835. doi: 10.1084/jem.158.3.822. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swain S. L., McKenzie D. T., Dutton R. W., Tonkonogy S. L., English M. The role of IL4 and IL5: characterization of a distinct helper T cell subset that makes IL4 and IL5 (Th2) and requires priming before induction of lymphokine secretion. Immunol Rev. 1988 Feb;102:77–105. doi: 10.1111/j.1600-065x.1988.tb00742.x. [DOI] [PubMed] [Google Scholar]
- Takahashi T., Yamaguchi N., Mita S., Yamaguchi Y., Suda T., Tominaga A., Kikuchi Y., Miura Y., Takatsu K. Structural comparison of murine T-cell (B151K12)-derived T-cell-replacing factor (IL-5) with rIL-5: dimer formation is essential for the expression of biological activity. Mol Immunol. 1990 Sep;27(9):911–920. doi: 10.1016/0161-5890(90)90158-v. [DOI] [PubMed] [Google Scholar]
- Takatsu K., Kikuchi Y., Takahashi T., Honjo T., Matsumoto M., Harada N., Yamaguchi N., Tominaga A. Interleukin 5, a T-cell-derived B-cell differentiation factor also induces cytotoxic T lymphocytes. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4234–4238. doi: 10.1073/pnas.84.12.4234. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takatsu K., Tanaka K., Tominaga A., Kumahara Y., Hamaoka T. Antigen-induced T cell-replacing factor (TRF). III. Establishment of T cell hybrid clone continuously producing TRF and functional analysis of released TRF. J Immunol. 1980 Dec;125(6):2646–2653. [PubMed] [Google Scholar]
- Takatsu K., Tominaga A., Harada N., Mita S., Matsumoto M., Takahashi T., Kikuchi Y., Yamaguchi N. T cell-replacing factor (TRF)/interleukin 5 (IL-5): molecular and functional properties. Immunol Rev. 1988 Feb;102:107–135. doi: 10.1111/j.1600-065x.1988.tb00743.x. [DOI] [PubMed] [Google Scholar]
- Takatsu K., Yamaguchi N., Hitoshi Y., Sonoda E., Mita S., Tominaga A. Signal transduction through interleukin-5 receptors. Cold Spring Harb Symp Quant Biol. 1989;54(Pt 2):745–751. doi: 10.1101/sqb.1989.054.01.088. [DOI] [PubMed] [Google Scholar]
- Tominaga A., Matsumoto M., Harada N., Takahashi T., Kikuchi Y., Takatsu K. Molecular properties and regulation of mRNA expression for murine T cell-replacing factor/IL-5. J Immunol. 1988 Feb 15;140(4):1175–1181. [PubMed] [Google Scholar]
- Tominaga A., Mita S., Kikuchi Y., Hitoshi Y., Takatsu K., Nishikawa S., Ogawa M. Establishment of IL-5-dependent early B cell lines by long-term bone marrow cultures. Growth Factors. 1989;1(2):135–146. doi: 10.3109/08977198909029123. [DOI] [PubMed] [Google Scholar]
- Tominaga A., Takahashi T., Kikuchi Y., Mita S., Naomi S., Harada N., Yamaguchi N., Takatsu K. Role of carbohydrate moiety of IL-5. Effect of tunicamycin on the glycosylation of IL-5 and the biologic activity of deglycosylated IL-5. J Immunol. 1990 Feb 15;144(4):1345–1352. [PubMed] [Google Scholar]
- Yamaguchi N., Hitoshi Y., Mita S., Hosoya Y., Murata Y., Kikuchi Y., Tominaga A., Takatsu K. Characterization of the murine interleukin 5 receptor by using a monoclonal antibody. Int Immunol. 1990;2(2):181–187. doi: 10.1093/intimm/2.2.181. [DOI] [PubMed] [Google Scholar]
- Yamaguchi Y., Suda T., Suda J., Eguchi M., Miura Y., Harada N., Tominaga A., Takatsu K. Purified interleukin 5 supports the terminal differentiation and proliferation of murine eosinophilic precursors. J Exp Med. 1988 Jan 1;167(1):43–56. doi: 10.1084/jem.167.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamasaki K., Taga T., Hirata Y., Yawata H., Kawanishi Y., Seed B., Taniguchi T., Hirano T., Kishimoto T. Cloning and expression of the human interleukin-6 (BSF-2/IFN beta 2) receptor. Science. 1988 Aug 12;241(4867):825–828. doi: 10.1126/science.3136546. [DOI] [PubMed] [Google Scholar]
- Yokota T., Coffman R. L., Hagiwara H., Rennick D. M., Takebe Y., Yokota K., Gemmell L., Shrader B., Yang G., Meyerson P. Isolation and characterization of lymphokine cDNA clones encoding mouse and human IgA-enhancing factor and eosinophil colony-stimulating factor activities: relationship to interleukin 5. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7388–7392. doi: 10.1073/pnas.84.21.7388. [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]