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Thromb Haemost 2008; 99(05): 863-873
DOI: 10.1160/TH07-11-0703
Theme Issue Article
Schattauer GmbH

Haematopoietic growth factors and their therapeutic use

Meenu Wadhwa
1   Biotherapeutics Group, National Institute for Biological Standards and Control, Blanche Lane, South Mimms, Potters Bar, Hertfordshire, United Kingdom
,
Robin Thorpe
1   Biotherapeutics Group, National Institute for Biological Standards and Control, Blanche Lane, South Mimms, Potters Bar, Hertfordshire, United Kingdom
› Author Affiliations
Further Information

Publication History

Received 27 November 2007

Accepted after minor revision 25 January 2008

Publication Date:
30 November 2017 (online)

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Summary

Haematopoietic growth factors constitute an important group of proteins that predominantly regulate the process of haematopoiesis. While some of these proteins have a very broad array of action on very early haematopoietic progenitors leading to multi-lineage increases in haematopoietic cell production and differentiation, others act in a restricted manner on specific committed terminally differentiated cell types. On the basis of their unique spectrum of activities, several factors are approved for clinical use in various indications while others are under investigation in the clinic either alone or as combination therapy. In this review, we have described factors which directly and in some cases indirectly influence haematopoiesis with particular focus on those factors which are either approved or show potential for clinical use. A brief description of the products that are currently available for clinical use is also provided. At present, several new products which include fusion proteins, peptide mimetics are either at the pre-clinical stage or in clinical development for various indications and these are also briefly described.

Keywords

Haematopoiesis - second-generation - biosimilars - stem cells - adverse
 

  • References

  • 1 Nicola NA. et al. Purification of a factor inducing differentiation in murine myelomonocytic leukemia cells. Identification as granulocyte colony-stimulating factor. J Biol Chem 1983; 258: 9017-9023.
    PubMedGoogle Scholar
  • 2 Welte K. et al. Purification and biochemical characterization of human pluripotent hematopoietic colony- stimulating factor. Proc Natl Acad Sci USA 1985; 82: 1526-1530.
    CrossrefPubMedGoogle Scholar
  • 3 Nomura H. et al. Purification and characterization of human granulocyte colony-stimulating factor (G-CSF). EMBO J 1986; 5: 871-876.
    PubMedGoogle Scholar
  • 4 Nagata S. et al. Molecular cloning and expression of cDNA for human granulocyte colony-stimulating factor. Nature 1986; 319: 415-418.
    CrossrefPubMedGoogle Scholar
  • 5 Souza LM. et al. Recombinant human granulocyte colony-stimulating factor: effects on normal and leukemic myeloid cells. Science 1986; 232: 61-65.
    CrossrefPubMedGoogle Scholar
  • 6 Nicola NA. Hemopoietic cell growth factors and their receptors. Annu Rev Biochem 1989; 58: 45-77.
    CrossrefPubMedGoogle Scholar
  • 7 Demetri GD, Griffin JD. Granulocyte colony-stimulating factor and its receptor. Blood 1991; 78: 2791-2808.
    CrossrefPubMedGoogle Scholar
  • 8 Platzer E. Human hemopoietic growth factors. Eur J Haematol 1989; 42: 1-15.
    PubMedGoogle Scholar
  • 9 Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993; 81: 2844-2853.
    PubMedGoogle Scholar
  • 10 Rutella S. et al. Granulocyte colony-stimulating factor promotes the generation of regulatory DC through induction of IL-10 and IFN-alpha. Eur J Immunol 2004; 34: 1291-1302.
    CrossrefPubMedGoogle Scholar
  • 11 Lieschke GJ, Burgess AW. Granulocyte colony-stimulating factor and granulocyte-macrophage colony- stimulating factor (1). N Engl J Med 1992; 327: 28-35.
    CrossrefPubMedGoogle Scholar
  • 12 Lieschke GJ, Burgess AW. Granulocyte colony-stimulating factor and granulocyte-macrophage colony- stimulating factor (2). N Engl J Med 1992; 327: 99-106.
    CrossrefPubMedGoogle Scholar
  • 13 Ozer H. et al. Update of recommendations for the use of hematopoietic colony-stimulating factors: evidence- based, clinical practice guidelines. American Society of Clinical Oncology Growth Factors Expert Panel. J Clin Oncol 2000; 18: 3558-3585.
    CrossrefPubMedGoogle Scholar
  • 14 Roberts AW. G-CSF:. a key regulator of neutrophil production, but that’s not all! Growth Factors 2005; 23: 33-41.
    PubMedGoogle Scholar
  • 15 Heuser M. et al. Use of colony-stimulating factors for chemotherapy-associated neutropenia: review of current guidelines. Semin Hematol 2007; 44: 148-156.
    CrossrefPubMedGoogle Scholar
  • 16 Ottmann OG. et al. Current status of growth factors in the treatment of acute myeloid and lymphoblastic leukemia. Semin Hematol 2007; 44: 183-192.
    CrossrefPubMedGoogle Scholar
  • 17 Dührsen U. et al. Effects of recombinant human granulocyte colony-stimulating factor on hematopoietic progenitor cells in cancer patients. Blood 1988; 72: 2074-2081.
    PubMedGoogle Scholar
  • 18 Möhle R, Kanz L. Hematopoietic growth factors for hematopoietic stem cell mobilization and expansion. Semin Hematol 2007; 44: 193-202.
    CrossrefPubMedGoogle Scholar
  • 19 Ings SJ. et al. Peripheral blood stem cell yield in 400 normal donors mobilised with granulocyte colony-stimulating factor (G-CSF): impact of age, sex, donor weight and type of G-CSF used. Br J Haematol 2006; 134: 517-525.
    CrossrefPubMedGoogle Scholar
  • 20 Oh-eda M. et al. O-Linked sugar chain of human granulocyte stimulating factor protects it against polymerisation and denaturation allowing it to retain its biological activity. J Biol Chem 1990; 265: 11432-11435.
    PubMedGoogle Scholar
  • 21 Balaguer H. et al. Splenic rupture after granulocyte- colony-stimulating factor mobilization in a peripheral blood progenitor cell donor. Transfusion 2004; 44: 1260-1261.
    CrossrefPubMedGoogle Scholar
  • 22 Tigue CC. et al. Granulocyte-colony stimulating factor administration to healthy individuals and persons with chronic neutropenia or cancer: an overview of safety considerations from the Research on Adverse Drug Events and Reports project. Bone Marrow Transplant 2007; 40: 185-192.
    CrossrefPubMedGoogle Scholar
  • 23 Graber SE, Krantz SB. Erythropoietin and the control of red cell production. Annu Rev Med 1978; 29: 51-66.
    CrossrefPubMedGoogle Scholar
  • 24 Lin FK. et al. Cloning and expression of the human erythropoietin gene. Proc Natl Acad Sci USA 1985; 82: 7580-7584.
    CrossrefPubMedGoogle Scholar
  • 25 Constantinescu SN. et al. The erythropoietin receptor: Structure, activation and intracellular signal transduction. Trends Endocrinol Metab 1999; 10: 18-23.
    CrossrefPubMedGoogle Scholar
  • 26 Takeuchi M. et al. Role of sugar chains in the in vitro biological activity of human erythropoietin produced in recombinant Chinese hamster ovary cells. J Biol Chem 1990; 265: 12127-12130.
    PubMedGoogle Scholar
  • 27 Lukowsky WA, Painter RH. Studies on the role of sialic acid in the physical and biological properties of erythropoietin. Can J Biochem 1972; 50: 909-917.
    CrossrefPubMedGoogle Scholar
  • 28 Eschbach JW. et al. Correction of the anemia of end-stage renal disease with recombinant human erythropoietin. Results of a combined phase I and II clinical trial. N Engl J Med 1987; 316: 73-78.
    CrossrefPubMedGoogle Scholar
  • 29 de Campos E. et al. Clinical and in vitro effects of recombinant human erythropoietin in patients receiving intensive chemotherapy for small-cell lung cancer. J Clin Oncol 1995; 13: 1623-1631.
    CrossrefPubMedGoogle Scholar
  • 30 Osterborg A. et al. Recombinant human erythropoietin in transfusion-dependent anemic patients with multiple myeloma and non-Hodgkin’s lymphoma–a randomized multicenter study. The European Study Group of Erythropoietin (Epoetin Beta) Treatment in Multiple Myeloma and Non-Hodgkin’s Lymphoma. Blood 1996; 87: 2675-2682.
    PubMedGoogle Scholar
  • 31 Means RT. Jr et al. Treatment of the anemia of rheumatoid arthritis with recombinant human erythropoietin: clinical and in vitro studies. Arthritis Rheum 1989; 32: 638-642.
    CrossrefPubMedGoogle Scholar
  • 32 Egrie JC, Browne JK. Development and characterization of novel erythropoiesis stimulating protein (NESP). Br J Cancer 2001; 84 (Suppl. 01) 3-10.
    CrossrefPubMedGoogle Scholar
  • 33 Elliott S. et al. Enhancement of therapeutic protein in vivo activities through glycoengineering. Nat Biotechnol 2003; 21: 414-421.
    CrossrefPubMedGoogle Scholar
  • 34 Casadevall N. et al. Pure red-cell aplasia and antierythropoietin antibodies in patients treated with recombinant erythropoietin. N Engl J Med 2002; 346: 469-475.
    CrossrefPubMedGoogle Scholar
  • 35 Metcalf D. et al. Biologic properties in vitro of a recombinant human granulocyte-macrophage colony-stimulating factor. Blood 1986; 67: 37-45.
    PubMedGoogle Scholar
  • 36 Ruef C, Coleman DL. Granulocyte-macrophage colony-stimulating factor: pleiotropic cytokine with potential clinical usefulness. Rev Infect Dis 1990; 12: 41-62.
    CrossrefPubMedGoogle Scholar
  • 37 Jones TC. The effect of granulocyte-macrophage colony stimulating factor (rGM-CSF) on macrophage function in microbial disease. Med Oncol 1996; 13: 141-147.
    CrossrefPubMedGoogle Scholar
  • 38 Caux C. et al. GM-CSF and TNF-alpha cooperate in the generation of dendritic Langerhans cells. Nature 1992; 360: 258-261.
    CrossrefPubMedGoogle Scholar
  • 39 Wong GG. et al. Human GM-CSF: molecular cloning of the complementary DNA and purification of the natural and recombinant proteins. Science 1985; 228: 810-815.
    CrossrefPubMedGoogle Scholar
  • 40 Lee F. et al. Isolation of cDNA for a human granulocyte- macrophage colony-stimulating factor by functional expression in mammalian cells. Proc Natl Acad Sci USA 1985; 82: 4360-4364.
    CrossrefPubMedGoogle Scholar
  • 41 Gearing DP. et al. Expression cloning of a receptor for human granulocyte-macrophage colony-stimulating factor. EMBO J 1989; 8: 3667-3676.
    PubMedGoogle Scholar
  • 42 Hayashida K. et al. Molecular cloning of a second subunit of the receptor for human granulocyte-macrophage colony-stimulating factor (GM-CSF): reconstitution of a high-affinity GM-CSF receptor. Proc Natl Acad Sci USA 1990; 87: 9655-9659.
    CrossrefPubMedGoogle Scholar
  • 43 Gerhartz HH. et al. Randomized, double-blind, placebo-controlled, phase III study of recombinant human granulocyte-macrophage colony-stimulating factor as adjunct to induction treatment of high-grade malignant non-Hodgkin’s lymphomas. Blood 1993; 82: 2329-2339.
    PubMedGoogle Scholar
  • 44 Mellstedt H. et al. Augmentation of the immune response with granulocyte-macrophage colony-stimulating factor and other hematopoietic growth factors. Curr Opin Hematol 1999; 6: 169-175.
    CrossrefPubMedGoogle Scholar
  • 45 Lieschke GJ. et al. Effects of bacterially synthesized recombinant human granulocyte-macrophage colony-stimulating factor in patients with advanced malignancy. Ann Intern Med 1989; 110: 357-364.
    CrossrefPubMedGoogle Scholar
  • 46 Wadhwa M. et al. Production of neutralizing granulocyte- macrophage colony-stimulating factor (GMCSF) antibodies in carcinoma patients following GMCSF combination therapy. Clin Exp Immunol 1996; 104: 351-358.
    CrossrefPubMedGoogle Scholar
  • 47 Wadhwa M. et al. Immunogenicity of granulocytemacrophage colony-stimulating factor (GM-CSF) products in patients undergoing combination therapy with GM-CSF. Clin Cancer Res 1999; 5: 1353-1361.
    PubMedGoogle Scholar
  • 48 Huang E. et al. The hematopoietic growth factor KL is encoded by the Sl locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell 1990; 63: 225-233.
    CrossrefPubMedGoogle Scholar
  • 49 Williams DE. et al. Identification of a ligand for the c-kit proto-oncogene. Cell 1990; 63: 167-174.
    CrossrefPubMedGoogle Scholar
  • 50 Zsebo KM. et al. Identification, purification, and biological characterization of hematopoietic stem cell factor from buffalo rat liver–conditioned medium. Cell 1990; 63: 195-201.
    CrossrefPubMedGoogle Scholar
  • 51 Huang EJ. et al. Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol Biol Cell 1992; 3: 349-362.
    CrossrefPubMedGoogle Scholar
  • 52 Arakawa T. et al. Glycosylated and unglycosylated recombinant-derived human stem cell factors are dimeric and have extensive regular secondary structure. J Biol Chem 1991; 266: 18942-18948.
    PubMedGoogle Scholar
  • 53 Broudy VC. Stem cell factor and hematopoiesis. Blood 1997; 90: 1345-1364.
    PubMedGoogle Scholar
  • 54 Glaspy JA. et al. Peripheral blood progenitor cell mobilization using stem cell factor in combination with filgrastim in breast cancer patients. Blood 1997; 9: 2939-2951.
    PubMedGoogle Scholar
  • 55 To LB. et al. Successful mobilization of peripheral blood stem cells after addition of ancestim (stem cell factor) in patients who had failed a prior mobilization with filgrastim (granulocyte colony-stimulating factor) alone or with chemotherapy plus filgrastim. Bone Marrow Transplant 2003; 31: 371-378.
    CrossrefPubMedGoogle Scholar
  • 56 Jensen BM. et al. Targeting kit activation: a potential therapeutic approach in the treatment of allergic inflammation. Inflamm Allergy Drug Targets 2007; 6: 57-62.
    CrossrefPubMedGoogle Scholar
  • 57 Paul SR. et al. Molecular cloning of a cDNA encoding interleukin 11, a stromal cell-derived lymphopoietic and hematopoietic cytokine. Proc Natl Acad Sci USA 1990; 87: 7512-7516.
    CrossrefPubMedGoogle Scholar
  • 58 Turner KJ, Clark SC. Interleukin-11; biological and clinical perspectives. Hematopoietic growth factors in clinical applications.. Marcel Dekker; 1995: 315-336.
    Google Scholar
  • 59 Du XX, Williams DA. Interleukin-11: a multifunctional growth factor derived from the hematopoietic microenvironment. Blood 1994; 83: 2023-2030.
    PubMedGoogle Scholar
  • 60 Paul SR, Schendel P. The cloning and biological characterization of recombinant human interleukin 11. Int J Cell Cloning 1992; 10: 135-143.
    PubMedGoogle Scholar
  • 61 Quesniaux VF. et al. Interleukin-11 stimulates multiple phases of erythropoiesis in vitro. Blood 1992; 80: 1218-1223.
    PubMedGoogle Scholar
  • 62 Gordon MS. et al. A phase I trial of recombinant human interleukin-11 (neumega rhIL-11 growth factor) in women with breast cancer receiving chemotherapy. Blood 1996; 87: 3615-3624.
    PubMedGoogle Scholar
  • 63 Kaye JA. FDA licensure of NEUMEGA to prevent severe chemotherapy-induced thrombocytopenia. Stem Cells 1998; 16 (Suppl. 02) 207-223.
    CrossrefPubMedGoogle Scholar
  • 64 Kaushansky K. Thrombopoietin. N Engl J Med 1998; 339: 746-754.
    CrossrefPubMedGoogle Scholar
  • 65 de Sauvage FJ. et al. Stimulation of megakaryocytopoiesis and thrombopoiesis by the c-Mpl ligand. Nature 1994; 369: 533-538.
    CrossrefPubMedGoogle Scholar
  • 66 Kaushansky K. et al. Promotion of megakaryocyte progenitor expansion and differentiation by the c-Mpl ligand thrombopoietin. Nature 1994; 369: 568-571.
    CrossrefPubMedGoogle Scholar
  • 67 Lok S. et al. Cloning and expression of murine thrombopoietin cDNA and stimulation of platelet production in vivo. Nature 1994; 369: 565-58.
    CrossrefPubMedGoogle Scholar
  • 68 Broudy VC. et al. Human platelets display high-affinity receptors for thrombopoietin. Blood 1997; 89: 1896-1904.
    PubMedGoogle Scholar
  • 69 Fielder PJ. et al. Human platelets as a model for the binding and degradation of thrombopoietin. Blood 1997; 89: 2782-2788.
    PubMedGoogle Scholar
  • 70 Deutsch VR, Tomer A. Megakaryocyte development and platelet production. Br J Haematol 2006; 134: 453-466.
    CrossrefPubMedGoogle Scholar
  • 71 Kaushansky K. Lineage-specific hematopoietic growth factors. N Engl J Med 2006; 354: 2034-2045.
    CrossrefPubMedGoogle Scholar
  • 72 Yang M. et al. Expression of interleukin (IL) 1 type I and type II receptors in megakaryocytic cells and enhancing effects of IL-1beta on megakaryocytopoiesis and NF-E2 expression. Br J Haematol 2000; 111: 371-380.
    CrossrefPubMedGoogle Scholar
  • 73 Kaushansky K. Thrombopoietin and the hematopoietic stem cell. Ann NY Acad Sci 2005; 1044: 139-141.
    CrossrefPubMedGoogle Scholar
  • 74 Ivanovic Z. et al. A clinical-scale expansion of mobilized CD 34+ hematopoietic stem and progenitor cells by use of a new serum-free medium. Transfusion 2006; 46: 126-131.
    CrossrefPubMedGoogle Scholar
  • 75 Begley CG, Basser RL. Biologic and structural differences of thrombopoietic growth factors. Semin Hematol 2000; 37: 19-27.
    PubMedGoogle Scholar
  • 76 Kuter DJ. New thrombopoietic growth factors. Blood 2007; 109: 4607-4616.
    CrossrefPubMedGoogle Scholar
  • 77 Vadhan-Raj S. et al. Stimulation of megakaryocyte and platelet production by a single dose of recombinant human thrombopoietin in patients with cancer. Ann Intern Med 1997; 126: 673-681.
    CrossrefPubMedGoogle Scholar
  • 78 Li J. et al. Thrombocytopenia caused by the development of antibodies to thrombopoietin. Blood 2001; 98: 3241-3248.
    CrossrefPubMedGoogle Scholar
  • 79 Basser RL. et al. Development of pancytopenia with neutralizing antibodies to thrombopoietin after multicycle chemotherapy supported by megakaryocyte growth and development factor. Blood 2002; 99: 2599-2602.
    CrossrefPubMedGoogle Scholar
  • 80 Ciurea SO, Hoffman R. Cytokines for the treatment of thrombocytopenia. Semin Hematol 2007; 44: 166-182.
    CrossrefPubMedGoogle Scholar
  • 81 Bussel JB. et al. AMG 531, a thrombopoiesisstimulating protein, for chronic ITP. N Engl J Med 2006; 355: 1672-1681.
    CrossrefPubMedGoogle Scholar
  • 82 Bussel JB. et al. Eltrombopag for the treatment of chronic idiopathic thrombocytopenic purpura. N Engl J Med 2007; 357: 2237-2247.
    CrossrefPubMedGoogle Scholar
  • 83 Jenkins JM. et al. Phase 1 clinical study of eltrombopag, an oral, nonpeptide thrombopoietin receptor agonist. Blood 2007; 109: 4739-4741.
    CrossrefPubMedGoogle Scholar
  • 84 Stasi R. et al. Idiopathic thrombocytopenic purpura: Current concepts in pathophysiology and management. Thromb Haemost 2008; 99: 4-13.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 85 Clark SC, Kamen R. The human hematopoietic colony- stimulating factors. Science 1987; 236: 1229-1237.
    CrossrefPubMedGoogle Scholar
  • 86 Metcalf D. Control of granulocytes and macrophages: molecular, cellular, and clinical aspects. Science 1991; 254: 529-533.
    CrossrefPubMedGoogle Scholar
  • 87 Clark-Lewis I. et al. Purification to apparent homogeneity of a factor stimulating the growth of multiple lineages of hemopoietic cells. J Biol Chem 1984; 259: 7488-7494.
    PubMedGoogle Scholar
  • 88 Yang YC. et al. Human IL-3 (multi-CSF): identification by expression cloning of a novel hematopoietic growth factor related to murine IL-3. Cell 1986; 47: 3-10.
    CrossrefPubMedGoogle Scholar
  • 89 Leary AG. et al. Recombinant gibbon interleukin 3 supports formation of human multilineage colonies and blast cell colonies in culture: comparison with recombinant human granulocyte-macrophage colony-stimulating factor. Blood 1987; 70: 1343-1348.
    PubMedGoogle Scholar
  • 90 Kitamura T. et al. Expression cloning of the human IL-3 receptor cDNA reveals a shared beta subunit for the human IL-3 and GM-CSF receptors. Cell 1991; 66: 1165-1174.
    CrossrefPubMedGoogle Scholar
  • 91 Miyajima A. et al. Receptors for granulocyte-macrophage colony-stimulating factor, interleukin-3, and interleukin-5. Blood 1993; 82: 1960-1974.
    PubMedGoogle Scholar
  • 92 Platzer E. et al. Biological activities of a human pluripotent hemopoietic colony stimulating factor on normal and leukemic cells. J Exp Med 1985; 162: 1788-1801.
    CrossrefPubMedGoogle Scholar
  • 93 Eder M. et al. IL-3 in the clinic. Stem Cells 1997; 15: 327-333.
    CrossrefPubMedGoogle Scholar
  • 94 Ganser A. et al. Effects of recombinant human interleukin- 3 in patients with myelodysplastic syndromes. Blood 1990; 76: 455-462.
    PubMedGoogle Scholar
  • 95 Ganser A. et al. Effects of recombinant human interleukin- 3 in patients with normal hematopoiesis and in patients with bone marrow failure. Blood 1990; 76: 666-676.
    PubMedGoogle Scholar
  • 96 Kurzrock R. Thrombopoietic factors in chronic bone marrow failure states: the platelet problem revisited. Clin Cancer Res 2005; 11: 1361-1367.
    CrossrefPubMedGoogle Scholar
  • 97 Tushinski RJ. et al. Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell 1982; 28: 71-81.
    CrossrefPubMedGoogle Scholar
  • 98 Stanley ER. et al. CSF-1–a mononuclear phagocyte lineage-specific hemopoietic growth factor. J Cell Biochem 1983; 21: 151-159.
    CrossrefPubMedGoogle Scholar
  • 99 Ralph P, Sampson-Johannes A. Macrophage growth and stimulating factor, M-CSF. Prog Clin Biol Res 1990; 338: 43-63.
    PubMedGoogle Scholar
  • 100 Kirma N. et al. Elevated expression of the oncogene c-fms and its ligand, the macrophage colony-stimulating factor-1, in cervical cancer and the role of transforming growth factor-beta 1 in inducing c-fms expression. Cancer Res 2007; 67: 1918-1926.
    CrossrefPubMedGoogle Scholar
  • 101 Sherr CJ. Colony-stimulating factor-1 receptor. Blood 1990; 75: 1-12.
    PubMedGoogle Scholar
  • 102 Chitu V, Stanley ER. Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol 2006; 18: 39-48.
    CrossrefPubMedGoogle Scholar
  • 103 Dinarello CA. Interleukin-1 and interleukin-1 antagonism. Blood 1991; 77: 1627-1652.
    PubMedGoogle Scholar
  • 104 Oppenheim JJ, Gery I. Interleukin 1 is more than an interleukin. Immunol Today 1982; 3: 113-119.
    CrossrefPubMedGoogle Scholar
  • 105 Bagby GC. Jr. Interleukin-1 and hematopoiesis. Blood Rev 1989; 3: 152-161.
    CrossrefPubMedGoogle Scholar
  • 106 Smith KA. T-cell growth factor. Immunol Rev 1980; 51: 337-357.
    CrossrefPubMedGoogle Scholar
  • 107 Gearing A. et al. Human B cell proliferation is stimulated by interleukin 2. Immunol Lett 1985; 9: 105-108.
    CrossrefPubMedGoogle Scholar
  • 108 Robb R. Interleukin-2: the molecule and its function. Immunol Today 1984; 5: 203-209.
    CrossrefPubMedGoogle Scholar
  • 109 Trinchieri G. et al. Response of resting human peripheral blood natural killer cells to interleukin 2. J Exp Med 1984; 160: 1147-1169.
    CrossrefPubMedGoogle Scholar
  • 110 Callard RE. Immunoregulation by interleukin-4 in man. Br J Haematol 1991; 78: 293-299.
    CrossrefPubMedGoogle Scholar
  • 111 Yokota T. et al. Molecular biology of interleukin 4 and interleukin 5 genes and biology of their products that stimulate B cells, T cells and hemopoietic cells. Immunol Rev 1988; 102: 137-187.
    CrossrefPubMedGoogle Scholar
  • 112 Kishimoto T. The biology of interleukin-6. Blood 1989; 74: 1-10.
    PubMedGoogle Scholar
  • 113 Rennick D. et al. Interleukin-6 interacts with interleukin- 4 and other hematopoietic growth factors to selectively enhance the growth of megakaryocytic, erythroid, myeloid, and multipotential progenitor cells. Blood 1989; 73: 1828-1835.
    PubMedGoogle Scholar
  • 114 Clutterbuck E. et al. Recombinant human interleukin 5 is an eosinophil differentiation factor but has no activity in standard human B cell growth factor assays. Eur J Immunol 1987; 17: 1743-1750.
    CrossrefPubMedGoogle Scholar
  • 115 Clutterbuck EJ. et al. Human interleukin-5 (IL-5) regulates the production of eosinophils in human bone marrow cultures: comparison and interaction with IL-1, IL-3, IL-6, and GMCSF. Blood 1989; 73: 1504-1512.
    PubMedGoogle Scholar
  • 116 Namen AE. et al. B cell precursor growth-promoting activity. Purification and characterization of a growth factor active on lymphocyte precursors. J Exp Med 1988; 167: 988-1002.
    CrossrefPubMedGoogle Scholar
  • 117 Conlon PJ. et al. Murine thymocytes proliferate in direct response to interleukin-7. Blood 1989; 74: 1368-1373.
    PubMedGoogle Scholar
  • 118 Yang YC. et al. Expression cloning of cDNA encoding a novel human hematopoietic growth factor: human homologue of murine T-cell growth factor P40. Blood 1989; 74: 1880-1884.
    PubMedGoogle Scholar
  • 119 Kobayashi M. et al. Identification and purification of natural killer cell stimulatory factor (NKSF),a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 1989; 170: 827-845.
    CrossrefPubMedGoogle Scholar
  • 120 Lieberman MD. et al. Natural killer cell stimulatory factor (NKSF) augments natural killer cell and antibody-dependent tumoricidal response against colon carcinoma cell lines. J Surg Res 1991; 50: 410-415.
    CrossrefPubMedGoogle Scholar
  • 121 Carson WE. et al. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med 1994; 180: 1395-1403.
    CrossrefPubMedGoogle Scholar
  • 122 Grabstein KH. et al. Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science 1994; 264: 965-968.
    CrossrefPubMedGoogle Scholar
  • 123 Goey H. et al. Inhibition of early murine hemopoietic progenitor cell proliferation after in vivo locoregional administration of transforming growth factor-beta 1. J Immunol 1989; 143: 877-880.
    PubMedGoogle Scholar
  • 124 Rigby WF. et al. The effects of recombinant-DNAderived interferons on the growth of myeloid progenitor cells. Blood 1985; 65: 858-861.
    PubMedGoogle Scholar
  • 125 Naranda T. et al. Activation of erythropoietin receptor through a novel extracellular binding site. Endocrinology 2002; 143: 2293-2302.
    CrossrefPubMedGoogle Scholar
  • 126 Thorpe R, Wadhwa M. Protein therapeutics and their immunogenicity. Eur J Hosp Pharm Pract 2006; 12: 17-18.
    PubMedGoogle Scholar
  • 127 Wadhwa M, Thorpe R. Unwanted immunogenicity: Is it a problem for biosimilar products?. BIOforum Europe 2006; 10: 46-48.
    PubMedGoogle Scholar
  • 128 Wadhwa M, Thorpe R. Unwanted immunogenicity: Implications for follow-on biologicals. Drug Inf J 2007; 41: 1-10.
    CrossrefPubMedGoogle Scholar
  • 129 Mellstedt H. et al. The challenge of biosimilars. Ann Oncol 2007 Epub ahead of print.
    PubMedGoogle Scholar