G-CSF. Structure. Main activities and pathophysiological roles. Discovery. Accession numbers. Chromosome location
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1 G-CSF Shigekazu Nagata* Department of Genetics, Osaka University Medical School, 2-2 Yamada-oka Suita, Osaka, , Japan * corresponding author tel: , fax: , nagata@genetic.med.osaka-u.ac.jp DOI: /rwcy SUMMARY G-CSF is a 20±25 kda glycoprotein that specifically regulates the production of neutrophilic G granulocytes as well as enhancing the functional activities of mature neutrophils. It is produced by activated macrophages, endothelial cells, and fibroblasts. G-CSF is widely used clinically in the treatment of patients with neutropenia after cancer chemotherapy. BACKGROUND Discovery G-CSF (granulocyte colony-stimulating factor) was discovered in serum from endotoxin-treated mice as a factor that stimulates neutrophilic colony formation from bone marrow cells, and that induces differentiation of mouse WEHI-3B D cells into neutrophilic granulocytes (Nicola et al., 1983). Some human cell lines such as squamous carcinoma CHU-2 and bladder carcinoma 5637 were found to constitutively produce G-CSF (Welte et al., 1985; Nomura et al., 1986), and its cdna was cloned from these cell lines (Nagata et al., 1986a,b; Souza et al., 1986). Subsequently, mouse G-CSF was identified from a mouse NFSA cdna library by crosshybridization with human cdna (Tsuchiya et al., 1986). Alternative names G-CSF has also been known as colony-stimulating factor 3 (CSF-3), macrophage and granulocyte inducer type 1, granulocyte (MGI-1G), granulocyte-macrophage colony-stimulating factor (GM-CSF), and pluripotent colony-stimulating factor (pluripoietin). Structure G-CSF is a 20±25 kda glycoprotein. Main activities and pathophysiological roles G-CSF regulates production of neutrophilic granulocytes, and activates mature neutrophils. GENE AND GENE REGULATION Accession numbers Human G-CSF: M13008 (Nagata et al., 1986a,b; Souza et al., 1986) Murine G-CSF: M13926 (Tsuchiya et al., 1986) Chromosome location Human chromosome 17q21-q22 (Kanda et al., 1987) Mouse chromosome 11 (Buchberg et al., 1988) Regulatory sites and corresponding transcription factors There are three regulatory sequences (GPE, G-CSF promoter element) in the 300 bp upstream from the transcription initiation site. GPE1 contains ciselements for NFB and NF-IL6, while GPE2 is a typical cis-element for OCT (octamer) transcription factor (Nishizawa and Nagata, 1990; Nishizawa et al.,
2 936 Shigekazu Nagata 1990). Accordingly, fibroblasts from NF-IL6-deficient mice do not produce G-CSF upon stimulation by IL-6 or TNF. Cells and tissues that express the gene The G-CSF gene is expressed in monocytes, macrophages, endothelial cells, and fibroblasts. PROTEIN Accession numbers Human G-CSF: PID g117564; SwissProt P09919 (Nagata et al., 1986a,b; Souza et al., 1986) Mouse G-CSF: PID g117565; SwissProt P09920 (Tsuchiya et al., 1986) Sequence See Figure 1. Description of protein The N-terminal 30 amino acids serve as a signal sequence for secretion. Cys36 and Cys42, as well as Cys67 and Cys77, are connected by disulfide bonds (Lu et al., 1989). The isoelectric point of the protein is 5.5±6.1, depending on the degree of sialylation (Nomura et al., 1986). It is relatively stable to extreme ph levels (ph 2 or ph 10), temperature (50% loss of the activity at 70 C for 30 min), and strong denaturation agents (6 M guanidine hydrochloride, 8 M urea, 0.1% SDS) (Nicola et al., 1983). Discussion of crystal structure G-CSF has a four helix bundle structure (Hill et al., 1993; Lovejoy et al., 1993; Zink et al., 1994). Important homologies Human and mouse G-CSFs are 73.6% identical at the amino acid sequence level (Tsuchiya et al., 1986). There is a significant sequence homology between G-CSF and IL-6 (Hirano et al., 1986). The tertiary structure of human G-CSF is similar to those of IL-4, IL-2, and growth hormone although the similarity in the primary sequence is not significant (Hill et al., 1993; Lovejoy et al., 1993; Zink et al., 1994). Posttranslational modifications Human G-CSF is O-glycosylated at Thr133. The structure of the sugar moiety attached to human G- CSF is N-acetylneuraminic acid (2-6)[galactose (1-3)] N-acetylgalactosamine (Souza et al., 1986; Oheda et al., 1990). CELLULAR SOURCES AND TISSUE EXPRESSION Cellular sources that produce Monocytes, macrophages, endothelial cells, and fibroblasts are induced to express G-CSF by various stimuli (Metcalf and Nicola, 1985; Broudy et al., 1987; Koeffler et al., 1987; Seelentag et al., 1987; Kaushansky et al., 1988; Lu et al., 1988; Vellenga et al., 1988; Nishizawa and Nagata, 1990). Some carcinoma cells, such as human squamous carcinoma CHU-2, bladder carcinoma 5637, glioblastoma U87MG, and hepatoma SK-HEP-1 cell lines produce G-CSF constitutively (Nomura et al., 1986; Tweardy et al., 1987). Eliciting and inhibitory stimuli, including exogenous and endogenous modulators TNF as well as IL-1 stimulate fibroblasts or endothelial cells to produce G-CSF (Broudy et al., Figure 1 Amino acid sequence for human G-CSF.
3 G-CSF ; Koeffler et al., 1987; Seelentag et al., 1987; Kaushansky et al., 1988). Endotoxins stimulate macrophages to produce G-CSF (Metcalf and Nicola, 1985; Nishizawa and Nagata, 1990). RECEPTOR UTILIZATION G-CSF has a unique receptor (G-CSF receptor). IN VITRO ACTIVITIES In vitro findings G-CSF stimulates the colony formation of neutrophilic granulocytes in semi-solid cultures of bone marrow cells (Nicola et al., 1983). Unlike other CSFs such as GM-CSF and IL-3, G-CSF is rather specific to progenitor cells of neutrophilic granulocytes. G- CSF stimulates not only proliferation and differentiation of the progenitors, but also prolongs the survival of the mature neutrophils and enhances the functional capacity of the mature neutrophils (Kitagawa et al., 1987; Williams et al., 1990; Yuo et al., 1989). Several myeloid leukemia cell lines such as mouse NFS60 and human TF-1 cells proliferate in response to G-CSF (Tsuchiya et al., 1986; Kitamura et al., 1989), whereas some other myeloid cell lines, such as mouse WEHI- 3B D, 32D, and L-G, can be induced to differentiate into neutrophilic granulocytes by G-CSF (Nicola et al., 1983; Valtieri et al., 1987; Lee et al., 1991). Regulatory molecules: Inhibitors and enhancers G-CSF-induced neutrophilic colony formation from bone marrow is inhibited by IFN, lymphotoxin, and TNF (Barber et al., 1987). also assayed by its ability to induce differentiation of WEHI-3B D or 32D cells into neutrophils. IN VIVO BIOLOGICAL ACTIVITIES OF LIGANDS IN ANIMAL MODELS Normal physiological roles The normal physiological role of G-CSF is the production of neutrophils. Species differences G-CSF has no species-specificity between human and mouse (Tsuchiya et al., 1986). Knockout mouse phenotypes Mice lacking the G-CSF gene show chronic neutropenia, are deficient in granulocyte and macrophage progenitor cells, and show impaired neutrophil mobilization (Lieschke et al., 1994). Transgenic overexpression Long-term exposure of mice to G-CSF in transgenic mice causes sustained granulocytosis (Chang et al., 1989). Pharmacological effects Administration of G-CSF into mice stimulates granulopoiesis (Cohen et al., 1987; Tsuchiya et al., 1987; Welte et al., 1987). Bioassays used G-CSF can be assayed by its neutrophilic colonystimulating activity in semi-solid culture of bone marrow cells. In this assay, G-CSF has a specific activity of about units/mg protein (where 50 units/ml is the concentration required for halfmaximal stimulation). G-CSF can be assayed by the MTT method, or [ 3 H]thymidine incorporation into G-CSF-responsive cells such as NFS-60 cells. It is PATHOPHYSIOLOGICAL ROLES IN NORMAL HUMANS AND DISEASE STATES AND DIAGNOSTIC UTILITY Normal levels and effects Serum of healthy persons contains less than 30 pg/ml of G-CSF. Its level increases to 50±2000 g/ml in
4 938 Shigekazu Nagata patients with acute bacterial infections. The G-CSF levels rise during the neutropenic phase of cyclic neutropenia (Watari et al., 1989). IN THERAPY Preclinical ± How does it affect disease models in animals? Administration of G-CSF protects neutropenic mice from lethal bacterial infection by accelerating recovery of neutrophils (Matsumoto et al., 1987). Effects of therapy: Cytokine, antibody to cytokine inhibitors, etc. G-CSF is effectively used to stimulate granulopoiesis in neutropenic patients. Pharmacokinetics The distribution half-life is about 30 minutes and the elimination half-life is about 3.8 hours in mice (Cohen et al., 1987). The elimination half-life in patients varies from less than an hour to several hours with some evidence that this is dependent on neutrophil numbers and receptor-mediated clearance (Watari et al., 1997). Toxicity No severe toxicity. Clinical results G-CSF is widely used clinically in patients with granulopenia from various causes (Ganser and Karthaus, 1996; Welte et al., 1996). G-CSF is administered to patients with cancer receiving chemotherapy or radiotherapy with or without bone marrow transplantation, and to patients receiving immunosuppressive agents after organ transplantation. In both types of patients, G-CSF accelerates the recovery of neutrophilic granulocytes and diminishes the risk of severe bacterial and fungal infections after chemotherapy. In addition, G-CSF is currently used to mobilize hematopoietic progenitor cells out of the bone marrow into the blood allowing autologous bone marrow transplantation (BMT) to be replaced by peripheral blood stem cell (PBSC) transplants. This procedure allows more rapid hematopoietic recovery than that seen by traditional BMT (Sheridan et al., 1992). G-CSF has also been used to treat patients with cyclic neutropenia. While it does not alter the cyclic nature of this disease, G-CSF elevates neutrophil levels during the nadir phase, thus preventing many of the symptoms of the disease (Hammond et al., 1989). References Barber, K. E., Crosier, P. S., and Watson, J. D. (1987). The differential inhibition of hemopoietic growth factor activity by cytotoxins and interferon-gamma. J. Immunol. 139, 1108±1112. Broudy, V. C., Kaushansky, K., Harlan, J. M., and Adamson, J. W. (1987). Interleukin 1 stimulates human endothelial cells to produce granulocyte-macrophage colonystimulating factor and granulocyte colony-stimulating factor. J. Immunol. 139, 464±468. Buchberg, A. M., Bedigian, H. G., Taylor, B. A., Brownell, E., Ihle, J. N., Nagata, S., Jenkins, N. A., and Copeland, N. G. (1988). Localization of Evi-2 to chromosome 11: Linkage to other proto-oncogene and growth factor loci using interspecific backcross mice. Oncogene Res. 2, 149±166. Chang, J. M., Metcalf, D., Gonda, T. J., and Johnson, G. R. (1989). Long-term exposure to retrovirally expressed granulocyte-colony-stimulating factor induces a nonneoplastic granulocytic and progenitor cell hyperplasia without tissue damage in mice. J. Clin. Invest. 84, 1488±1496. Cohen, A. M., Zsebo, K. M., Inoue, H., Hines, D., Boone, T. C., Chazin, V. R., Tsai, L., Ritch, T., and Souza, L. M. (1987). In vivo stimulating of granulopoiesis by recombinant human granulocyte colony-stimulating factor. Proc. Natl Acad. Sci. USA 84, 2484±2488. Ganser, A., and Karthaus, M. (1996). Clinical use of hematopoietic growth factors. Curr. Opin. Oncol. 8, 265±269. Hammond, W. P., Price, T. H., Souza, L. M., and Dale, D. C. (1989). Treatment of cyclic neutropenia with granulocyte colony-stimulating factor. N. Engl. J. Med. 320, 1306±1311. Hill, C. P., Osslund, T. D., and Eisenberg, D. (1993). The structure of granulocyte-colony-stimulating factor and its relationship to other growth factors. Proc. Natl Acad. Sci. USA 90, 5167±5171. Hirano, T., Yasukawa, K., Harada, H., Taga, T., Watanabe, Y., Matsuda, T., Kashiwamura, S., Nakajima, K., Koyama, K., Iwamatsu, A., Tsunasawa, S., Sakiyama, F., Matsui, H., Takahara, Y., Taniguchi, T., and Kishimoto, T. (1986). Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 324, 73±76. Kanda, N., Fukushige, S.-I., Murotsu, T., Yoshida, M. C., Tsuchiya, M., Asano, S., Kaziro, Y., and Nagata, S. (1987). Human gene coding for granulocyte colony-stimulating factor is assigned to the q21-q22 region of chromosome 17. Somat. Cell Mol. Genet. 13, 679±684. Kaushansky, K., Lin, N., and Adamson, J. W. (1988). Interleukin 1 stimulates fibroblasts to synthesize granulocyte-macrophage and granulocyte colony-stimulating factors. J. Clin. Invest. 81, 92±97. Kitagawa, S., Yuo, A., Souza, L. M., Saito, M., Miura, Y., and Takaku, F. (1987). Recombinant human granulocyte
5 G-CSF 939 colony-stimulating factor enhances superoxide release in human granulocytes stimulated by the chemotactic peptide. Biochem. Biophys. Res. Commun. 144, 1143±1146. Kitamura, T., Tange, T., Terasawa, T., Chiba, S., Kuwaki, T., Miyagawa, K., Piao, Y. F., Miyazono, K., Urabe, A., and Takaku, F. (1989). Establishment and characterization of a unique human cell line that proliferates dependently on GM- CSF, IL-3, or erythropoietin. J. Cell. Physiol. 140, 323±334. Koeffler, H. P., Gasson, J., Ranyard, J., Souza, L., Shepard, M., and Munker, R. (1987). Recombinant human TNF stimulates production of granulocyte colony-stimulating factor. Blood 70, 55±59. Lee, K. H., Kinashi, T., Tohyama, K., Tashiro, K., Funato, N., Hama, K., and Honjo, T. (1991). Different stromal cell lines support lineage-selective differentiation of the multipotential bone marrow stem cell clone LyD9. J. Exp. Med. 173, 1257±1266. Lieschke, G. J., Grail, D., Hodgson, G., Metcalf, D., Stanley, E., Cheers, C., Fowler, K. J., Basu, S., Zhan, Y. F., and Dunn, A. R. (1994). Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 84, 1737±1746. Lovejoy, B., Cascio, D., and Eisenberg, D. (1993). Crystal structure of canine and bovine granulocyte-colony stimulating factor (G-CSF). J. Mol. Biol. 234, 640±653. Lu, L., Walker, D., Graham, C. D., Waheed, A., Shadduck, R. K., and Broxmeyer, H. E. (1988). Enhancement of release from MHC class II antigen-positive monocytes of hematopoietic colony stimulating factors CSF-1 and G-CSF by recombinant human tumor necrosis factor-alpha: synergism with recombinant human interferon-gamma. Blood 72, 34±41. Lu, H. S., Boone, T. C., Souza, L. M., and Lai, P. H. (1989). Disulfide and secondary structures of recombinant human granulocyte colony stimulating factor. Arch. Biochem. Biophys. 268, 81±92. Matsumoto, M., Matsubara, S., Matsuno, T., Tamura, M., Hattori, K., Nomura, H., Ono, M., and Yokota, T. (1987). Protective effect of human granulocyte colony-stimulating factor on microbial infection in neutropenic mice. Infect. Immun. 55, 2715±2720. Metcalf, D., and Nicola, N. A. (1985). Synthesis by mouse peritoneal cells of G-CSF, the differentiation inducer for myeloid leukemia cells: Stimulation by endotoxin, M-CSF and multi- CSF. Leukemia Res. 1, 35±50. Nagata, S., Tsuchiya, M., Asano, S., Kaziro, Y., Yamazaki, T., Yamamoto, O., Hirata, Y., Kubota, N., Oheda, M., Nomura, H., and Ono, M. (1986a). Molecular cloning and expression of cdna for human granulocyte colony-stimulating factor. Nature 319, 415±418. Nagata, S., Tsuchiya, M., Asano, S., Yamamoto, O., Hirata, Y., Kubota, N., Oheda, M., Nomura, H., and Yamazaki, T. (1986b). The chromosomal gene structure and two mrnas for human granulocyte colony-stimulating factor. EMBO J. 5, 575±581. Nicola, N. A., Metcalf, D., Matsumoto, M., and Johnson, G. R. (1983). Purification of a factor inducing differentiation in murine myelomonocytic leukemia cells: identification as granulocyte colony-stimulating factor (G-CSF). J. Biol. Chem. 258, 9017± Nishizawa, M., and Nagata, S. (1990). Regulatory elements responsible for inducible expression of the granulocyte colonystimulating factor. Mol. Cell Biol. 10, 2002±2011. Nishizawa, M., Tsuchiya, M., Watanabe-Fukunaga, R., and Nagata, S. (1990). Multiple elements in the promoter of granulocyte colony-stimulating factor gene regulate its constitutive expression in human carcinoma cells. J. Biol. Chem. 265, 5897±5902. Nomura, H., Imazeki, I., Oheda, M., Kubota, N., Tamura, M., Ono, M., Ueyama, Y., and Asano, S. (1986). Purification and characterization of human granulocyte colony-stimulating factor (G-CSF). EMBO J. 5, 871±876. Oheda, M., Hasegawa, M., Hattori, K., Kuboniwa, H., Kojima, T., Orita, T., Tomonou, K., Yamazaki, T., and Ochi, N. (1990). O-linked sugar chain of human granulocyte colony-stimulating factor protects it against polymerization and denaturation allowing it to retain its biological activity. J. Biol. Chem. 265, 11432± Seelentag, W. K., Mermod, J.-J., Montesano, R., and Vassalli, P. (1987). Additive effects of interleukin 1 and tumor necrosis factor- on the accumulation of the three granulocyte and macrophage colony-stimulating factor mrnas in human endothelial cells. EMBO J. 6, 2261±2265. Sheridan, W. P., Begley, C. G., Juttner, C. A., Szer, J., To, L. B., Maher, D., McGrath, K. M., Morstyn, G., and Fox, R. M. (1992). Effect of peripheral-blood progenitor cells mobilised by filgrastim (G-CSF) on platelet recovery after high-dose chemotherapy. Lancet 339, 640±644. Souza, L. M., Boone, T. C., Gabrilove, J., Lai, P. H., Zsebo, K. M., Murdock, D. C., Chazin, V. R., Bruszewski, J., Lu, H., Chen, K. K., Barendt, J., Platzer, E., Moore, M. A. S., Mertelsmann, R., and Welte, K. (1986). 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Immunol. 138, 3829±3835. Vellenga, E., Rambaldi, A., Ernst, T. J., Ostapovicz, D., and Griffin, J. D. (1988). Independent regulation of M-CSF and G-CSF gene expression in human monocytes. Blood 71, 1529± Watari, K., Asano, S., Shirafuji, N., Kodo, H., Ozawa, K., Takaku, F., and Kamachi, S. (1989). Serum granulocyte colony-stimulating factor levels in healthy volunteers and patients with various disorders as estimated by enzyme immunoassay. Blood 73, 117±122. Watari, K., Ozawa, K., Takahashi, S., Tojo, A., Tani, K., Kamachi, S., and Asano, S. (1997). Pharmacokinetic studies of intravenous glycosylated recombinant human granulocyte colony-stimulating factor in various hematological disorders: inverse correlation between the half-life and bone marrow myeloid cell pool. Int. J. Hematol. 66, 57±67. Welte, K., Platzer, E., Lu, L., Gabrilove, J. L., Levi, E., Mertelsmann, R., and Moore, M. A. S. (1985). 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