Skip to main content
Environmental Health Perspectives logoLink to Environmental Health Perspectives
. 1989 Mar;80:199–207. doi: 10.1289/ehp.8980199

Hemopoietic stem cells: stochastic differentiation and humoral control of proliferation.

M Ogawa 1
PMCID: PMC1567604  PMID: 2647480

Abstract

The central feature of hemopoiesis is life-long, stable cell renewal. This process is supported by hemopoietic stem cells which, in the steady state, appear to be dormant in cell cycling. The entry into cell cycle of the dormant stem cells may be promoted by such factors as interleukin-1, interleukin-6 (IL-6), and granulocyte colony-stimulating factor (G-CSF). Once the stem cells leave G0 and begin proliferation, the subsequent process is characterized by continued proliferation and differentiation. While several models of stem cell differentiation have been proposed, micromanipulation studies of individual progenitors suggest that the commitment of multipotential progenitors to single lineages is a random (stochastic) process. The proliferation of early hemopoietic progenitors requires the presence of interleukin-3 (IL-3), and the intermediate process appears to be supported by granulocyte/macrophage colony-stimulating factor (GM-CSF). Once the progenitors are committed to individual lineages, the subsequent maturation process appears to be supported by late-acting, lineage-specific factors such as erythropoietin and G-CSF. Synthesis of a hemopoietic factor may take place in different cell types and is regulated by multiple factors. The physiological regulator of erythropoiesis is erythropoietin, which, by a feedback mechanism, provides fine control of erythrocyte production. Feedback mechanisms for leukocyte production have not been identified. It is possible that there is no feedback regulator of leukopoiesis. In this model, leukocyte production in the steady state is maintained at a genetically determined level. When an infection occurs, the bacterial lipopolysaccharides may augment the production of interleukin 1 alpha and beta, tumor necrosis factor, macrophage colony-stimulating factor, etc.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
199

Selected References

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

  1. BECKER A. J., MCCULLOCH E. A., SIMINOVITCH L., TILL J. E. THE EFFECT OF DIFFERING DEMANDS FOR BLOOD CELL PRODUCTION ON DNA SYNTHESIS BY HEMOPOIETIC COLONY-FORMING CELLS OF MICE. Blood. 1965 Sep;26:296–308. [PubMed] [Google Scholar]
  2. BRUCE W. R., MCCULLOCH E. A. THE EFFECT OF ERYTHROPOIETIC STIMULATION ON THE HEMOPOIETIC COLONY-FORMING CELLS OF MICE. Blood. 1964 Feb;23:216–232. [PubMed] [Google Scholar]
  3. Bagby G. C., Jr, Dinarello C. A., Wallace P., Wagner C., Hefeneider S., McCall E. Interleukin 1 stimulates granulocyte macrophage colony-stimulating activity release by vascular endothelial cells. J Clin Invest. 1986 Nov;78(5):1316–1323. doi: 10.1172/JCI112717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bartocci A., Pollard J. W., Stanley E. R. Regulation of colony-stimulating factor 1 during pregnancy. J Exp Med. 1986 Sep 1;164(3):956–961. doi: 10.1084/jem.164.3.956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Broudy V. C., Kaushansky K., Harlan J. M., Adamson J. W. Interleukin 1 stimulates human endothelial cells to produce granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor. J Immunol. 1987 Jul 15;139(2):464–468. [PubMed] [Google Scholar]
  6. Broudy V. C., Kaushansky K., Segal G. M., Harlan J. M., Adamson J. W. Tumor necrosis factor type alpha stimulates human endothelial cells to produce granulocyte/macrophage colony-stimulating factor. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7467–7471. doi: 10.1073/pnas.83.19.7467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burgess A. W., Camakaris J., Metcalf D. Purification and properties of colony-stimulating factor from mouse lung-conditioned medium. J Biol Chem. 1977 Mar 25;252(6):1998–2003. [PubMed] [Google Scholar]
  8. Cannistra S. A., Rambaldi A., Spriggs D. R., Herrmann F., Kufe D., Griffin J. D. Human granulocyte-macrophage colony-stimulating factor induces expression of the tumor necrosis factor gene by the U937 cell line and by normal human monocytes. J Clin Invest. 1987 Jun;79(6):1720–1728. doi: 10.1172/JCI113012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clark S. C., Kamen R. The human hematopoietic colony-stimulating factors. Science. 1987 Jun 5;236(4806):1229–1237. doi: 10.1126/science.3296190. [DOI] [PubMed] [Google Scholar]
  10. Cohen A. M., Zsebo K. M., Inoue H., Hines D., Boone T. C., Chazin V. R., Tsai L., Ritch T., Souza L. M. In vivo stimulation of granulopoiesis by recombinant human granulocyte colony-stimulating factor. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2484–2488. doi: 10.1073/pnas.84.8.2484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Curry J. L., Trentin J. J. Hemopoietic spleen colony studies. I. Growth and differentiation. Dev Biol. 1967 May;15(5):395–413. doi: 10.1016/0012-1606(67)90034-6. [DOI] [PubMed] [Google Scholar]
  12. Dancey J. T., Deubelbeiss K. A., Harker L. A., Finch C. A. Neutrophil kinetics in man. J Clin Invest. 1976 Sep;58(3):705–715. doi: 10.1172/JCI108517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dinarello C. A. Interleukin-1. Rev Infect Dis. 1984 Jan-Feb;6(1):51–95. doi: 10.1093/clinids/6.1.51. [DOI] [PubMed] [Google Scholar]
  14. Donahue R. E., Wang E. A., Stone D. K., Kamen R., Wong G. G., Sehgal P. K., Nathan D. G., Clark S. C. Stimulation of haematopoiesis in primates by continuous infusion of recombinant human GM-CSF. 1986 Jun 26-Jul 2Nature. 321(6073):872–875. doi: 10.1038/321872a0. [DOI] [PubMed] [Google Scholar]
  15. Eliason J. F. Granulocyte-macrophage colony formation in serum-free culture: effects of purified colony-stimulating factors and modulation by hydrocortisone. J Cell Physiol. 1986 Aug;128(2):231–238. doi: 10.1002/jcp.1041280214. [DOI] [PubMed] [Google Scholar]
  16. Eschbach J. W., Egrie J. C., Downing M. R., Browne J. K., Adamson J. W. 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 Jan 8;316(2):73–78. doi: 10.1056/NEJM198701083160203. [DOI] [PubMed] [Google Scholar]
  17. Fibbe W. E., van Damme J., Billiau A., Voogt P. J., Duinkerken N., Kluck P. M., Falkenburg J. H. Interleukin-1 (22-K factor) induces release of granulocyte-macrophage colony-stimulating activity from human mononuclear phagocytes. Blood. 1986 Dec;68(6):1316–1321. [PubMed] [Google Scholar]
  18. Fung M. C., Hapel A. J., Ymer S., Cohen D. R., Johnson R. M., Campbell H. D., Young I. G. Molecular cloning of cDNA for murine interleukin-3. Nature. 1984 Jan 19;307(5948):233–237. doi: 10.1038/307233a0. [DOI] [PubMed] [Google Scholar]
  19. Gabrilove J. L., Welte K., Harris P., Platzer E., Lu L., Levi E., Mertelsmann R., Moore M. A. Pluripoietin alpha: a second human hematopoietic colony-stimulating factor produced by the human bladder carcinoma cell line 5637. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2478–2482. doi: 10.1073/pnas.83.8.2478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gasson J. C., Weisbart R. H., Kaufman S. E., Clark S. C., Hewick R. M., Wong G. G., Golde D. W. Purified human granulocyte-macrophage colony-stimulating factor: direct action on neutrophils. Science. 1984 Dec 14;226(4680):1339–1342. doi: 10.1126/science.6390681. [DOI] [PubMed] [Google Scholar]
  21. Goldwasser E. Erythropoietin and the differentiation of red blood cells. Fed Proc. 1975 Dec;34(13):2285–2292. [PubMed] [Google Scholar]
  22. Gough N. M., Gough J., Metcalf D., Kelso A., Grail D., Nicola N. A., Burgess A. W., Dunn A. R. Molecular cloning of cDNA encoding a murine haematopoietic growth regulator, granulocyte-macrophage colony stimulating factor. 1984 Jun 28-Jul 4Nature. 309(5971):763–767. doi: 10.1038/309763a0. [DOI] [PubMed] [Google Scholar]
  23. Gregory C. J. Erythropoietin sensitivity as a differentiation marker in the hemopoietic system: studies of three erythropoietic colony responses in culture. J Cell Physiol. 1976 Oct;89(2):289–301. doi: 10.1002/jcp.1040890212. [DOI] [PubMed] [Google Scholar]
  24. Groopman J. E., Mitsuyasu R. T., DeLeo M. J., Oette D. H., Golde D. W. Effect of recombinant human granulocyte-macrophage colony-stimulating factor on myelopoiesis in the acquired immunodeficiency syndrome. N Engl J Med. 1987 Sep 3;317(10):593–598. doi: 10.1056/NEJM198709033171003. [DOI] [PubMed] [Google Scholar]
  25. Hamaguchi Y., Kanakura Y., Fujita J., Takeda S., Nakano T., Tarui S., Honjo T., Kitamura Y. Interleukin 4 as an essential factor for in vitro clonal growth of murine connective tissue-type mast cells. J Exp Med. 1987 Jan 1;165(1):268–273. doi: 10.1084/jem.165.1.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hara H., Ogawa M. Erythropoietic precursors in mice under erythropoietic stimulation and suppression. Exp Hematol. 1977 Mar;5(2):141–148. [PubMed] [Google Scholar]
  27. Hara H., Ogawa M. Murine hemopoietic colonies in culture containing normoblasts, macrophages, and megakaryocytes. Am J Hematol. 1978;4(1):23–34. doi: 10.1002/ajh.2830040105. [DOI] [PubMed] [Google Scholar]
  28. Hodgson G. S., Bradley T. R. Properties of haematopoietic stem cells surviving 5-fluorouracil treatment: evidence for a pre-CFU-S cell? Nature. 1979 Oct 4;281(5730):381–382. doi: 10.1038/281381a0. [DOI] [PubMed] [Google Scholar]
  29. Hoffman R., Yang H. H., Bruno E., Straneva J. E. Purification and partial characterization of a megakaryocyte colony-stimulating factor from human plasma. J Clin Invest. 1985 Apr;75(4):1174–1182. doi: 10.1172/JCI111813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Howard M., Farrar J., Hilfiker M., Johnson B., Takatsu K., Hamaoka T., Paul W. E. Identification of a T cell-derived b cell growth factor distinct from interleukin 2. J Exp Med. 1982 Mar 1;155(3):914–923. doi: 10.1084/jem.155.3.914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ihle J. N., Keller J., Henderson L., Klein F., Palaszynski E. Procedures for the purification of interleukin 3 to homogeneity. J Immunol. 1982 Dec;129(6):2431–2436. [PubMed] [Google Scholar]
  32. Ihle J. N., Keller J., Oroszlan S., Henderson L. E., Copeland T. D., Fitch F., Prystowsky M. B., Goldwasser E., Schrader J. W., Palaszynski E. Biologic properties of homogeneous interleukin 3. I. Demonstration of WEHI-3 growth factor activity, mast cell growth factor activity, p cell-stimulating factor activity, colony-stimulating factor activity, and histamine-producing cell-stimulating factor activity. J Immunol. 1983 Jul;131(1):282–287. [PubMed] [Google Scholar]
  33. Ikebuchi K., Clark S. C., Ihle J. N., Souza L. M., Ogawa M. Granulocyte colony-stimulating factor enhances interleukin 3-dependent proliferation of multipotential hemopoietic progenitors. Proc Natl Acad Sci U S A. 1988 May;85(10):3445–3449. doi: 10.1073/pnas.85.10.3445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ikebuchi K., Wong G. G., Clark S. C., Ihle J. N., Hirai Y., Ogawa M. Interleukin 6 enhancement of interleukin 3-dependent proliferation of multipotential hemopoietic progenitors. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9035–9039. doi: 10.1073/pnas.84.24.9035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Iscove N. N. The role of erythropoietin in regulation of population size and cell cycling of early and late erythroid precursors in mouse bone marrow. Cell Tissue Kinet. 1977 Jul;10(4):323–334. doi: 10.1111/j.1365-2184.1977.tb00300.x. [DOI] [PubMed] [Google Scholar]
  36. Jacobs K., Shoemaker C., Rudersdorf R., Neill S. D., Kaufman R. J., Mufson A., Seehra J., Jones S. S., Hewick R., Fritsch E. F. Isolation and characterization of genomic and cDNA clones of human erythropoietin. 1985 Feb 28-Mar 6Nature. 313(6005):806–810. doi: 10.1038/313806a0. [DOI] [PubMed] [Google Scholar]
  37. Jubinsky P. T., Stanley E. R. Purification of hemopoietin 1: a multilineage hemopoietic growth factor. Proc Natl Acad Sci U S A. 1985 May;82(9):2764–2768. doi: 10.1073/pnas.82.9.2764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kaushansky K., O'Hara P. J., Berkner K., Segal G. M., Hagen F. S., Adamson J. W. Genomic cloning, characterization, and multilineage growth-promoting activity of human granulocyte-macrophage colony-stimulating factor. Proc Natl Acad Sci U S A. 1986 May;83(10):3101–3105. doi: 10.1073/pnas.83.10.3101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kawasaki E. S., Ladner M. B., Wang A. M., Van Arsdell J., Warren M. K., Coyne M. Y., Schweickart V. L., Lee M. T., Wilson K. J., Boosman A. Molecular cloning of a complementary DNA encoding human macrophage-specific colony-stimulating factor (CSF-1). Science. 1985 Oct 18;230(4723):291–296. doi: 10.1126/science.2996129. [DOI] [PubMed] [Google Scholar]
  40. Kimura H., Finch C. A., Adamson J. W. Hematopoiesis in the rat: quantitation of hematopoietic progenitors and the response to iron deficiency anemia. J Cell Physiol. 1986 Feb;126(2):298–306. doi: 10.1002/jcp.1041260221. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. Koeffler H. P., Gasson J., Ranyard J., Souza L., Shepard M., Munker R. Recombinant human TNF alpha stimulates production of granulocyte colony-stimulating factor. Blood. 1987 Jul;70(1):55–59. [PubMed] [Google Scholar]
  43. Koike K., Ihle J. N., Ogawa M. Declining sensitivity to interleukin 3 of murine multipotential hemopoietic progenitors during their development. Application to a culture system that favors blast cell colony formation. J Clin Invest. 1986 Mar;77(3):894–899. doi: 10.1172/JCI112387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Koike K., Ogawa M., Ihle J. N., Miyake T., Shimizu T., Miyajima A., Yokota T., Arai K. Recombinant murine granulocyte-macrophage (GM) colony-stimulating factor supports formation of GM and multipotential blast cell colonies in culture: comparison with the effects of interleukin-3. J Cell Physiol. 1987 Jun;131(3):458–464. doi: 10.1002/jcp.1041310319. [DOI] [PubMed] [Google Scholar]
  45. Lajtha L. G. Stem cell concepts. Differentiation. 1979;14(1-2):23–34. doi: 10.1111/j.1432-0436.1979.tb01007.x. [DOI] [PubMed] [Google Scholar]
  46. Leary A. G., Ogawa M., Strauss L. C., Civin C. I. Single cell origin of multilineage colonies in culture. Evidence that differentiation of multipotent progenitors and restriction of proliferative potential of monopotent progenitors are stochastic processes. J Clin Invest. 1984 Dec;74(6):2193–2197. doi: 10.1172/JCI111645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Leary A. G., Strauss L. C., Civin C. I., Ogawa M. Disparate differentiation in hemopoietic colonies derived from human paired progenitors. Blood. 1985 Aug;66(2):327–332. [PubMed] [Google Scholar]
  48. Leary A. G., Yang Y. C., Clark S. C., Gasson J. C., Golde D. W., Ogawa M. 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 Nov;70(5):1343–1348. [PubMed] [Google Scholar]
  49. Lee F., Yokota T., Otsuka T., Meyerson P., Villaret D., Coffman R., Mosmann T., Rennick D., Roehm N., Smith C. Isolation and characterization of a mouse interleukin cDNA clone that expresses B-cell stimulatory factor 1 activities and T-cell- and mast-cell-stimulating activities. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2061–2065. doi: 10.1073/pnas.83.7.2061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Lemischka I. R., Raulet D. H., Mulligan R. C. Developmental potential and dynamic behavior of hematopoietic stem cells. Cell. 1986 Jun 20;45(6):917–927. doi: 10.1016/0092-8674(86)90566-0. [DOI] [PubMed] [Google Scholar]
  51. Lin F. K., Suggs S., Lin C. H., Browne J. K., Smalling R., Egrie J. C., Chen K. K., Fox G. M., Martin F., Stabinsky Z. Cloning and expression of the human erythropoietin gene. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7580–7584. doi: 10.1073/pnas.82.22.7580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Metcalf D., Johnson G. R., Burgess A. W. Direct stimulation by purified GM-CSF of the proliferation of multipotential and erythroid precursor cells. Blood. 1980 Jan;55(1):138–147. [PubMed] [Google Scholar]
  53. Metcalf D., Nicola N. A. Proliferative effects of purified granulocyte colony-stimulating factor (G-CSF) on normal mouse hemopoietic cells. J Cell Physiol. 1983 Aug;116(2):198–206. doi: 10.1002/jcp.1041160211. [DOI] [PubMed] [Google Scholar]
  54. Metcalf D. The granulocyte-macrophage colony-stimulating factors. Science. 1985 Jul 5;229(4708):16–22. doi: 10.1126/science.2990035. [DOI] [PubMed] [Google Scholar]
  55. Metcalf D. The molecular biology and functions of the granulocyte-macrophage colony-stimulating factors. Blood. 1986 Feb;67(2):257–267. [PubMed] [Google Scholar]
  56. Mintz B., Anthony K., Litwin S. Monoclonal derivation of mouse myeloid and lymphoid lineages from totipotent hematopoietic stem cells experimentally engrafted in fetal hosts. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7835–7839. doi: 10.1073/pnas.81.24.7835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Miyake T., Kung C. K., Goldwasser E. Purification of human erythropoietin. J Biol Chem. 1977 Aug 10;252(15):5558–5564. [PubMed] [Google Scholar]
  58. Mochizuki D. Y., Eisenman J. R., Conlon P. J., Larsen A. D., Tushinski R. J. Interleukin 1 regulates hematopoietic activity, a role previously ascribed to hemopoietin 1. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5267–5271. doi: 10.1073/pnas.84.15.5267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Moore M. A., Warren D. J. Synergy of interleukin 1 and granulocyte colony-stimulating factor: in vivo stimulation of stem-cell recovery and hematopoietic regeneration following 5-fluorouracil treatment of mice. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7134–7138. doi: 10.1073/pnas.84.20.7134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Motoyoshi K., Takaku F., Miura Y. High serum colony-stimulating activity of leukocytopenic patients after intravenous infusions of human urinary colony-stimulating factor. Blood. 1983 Sep;62(3):685–688. [PubMed] [Google Scholar]
  61. Munker R., Gasson J., Ogawa M., Koeffler H. P. Recombinant human TNF induces production of granulocyte-monocyte colony-stimulating factor. Nature. 1986 Sep 4;323(6083):79–82. doi: 10.1038/323079a0. [DOI] [PubMed] [Google Scholar]
  62. Nagao K., Yokoro K., Aaronson S. A. Continuous lines of basophil/mast cells derived from normal mouse bone marrow. Science. 1981 Apr 17;212(4492):333–335. doi: 10.1126/science.7209531. [DOI] [PubMed] [Google Scholar]
  63. Nagata S., Tsuchiya M., Asano S., Kaziro Y., Yamazaki T., Yamamoto O., Hirata Y., Kubota N., Oheda M., Nomura H. Molecular cloning and expression of cDNA for human granulocyte colony-stimulating factor. 1986 Jan 30-Feb 5Nature. 319(6052):415–418. doi: 10.1038/319415a0. [DOI] [PubMed] [Google Scholar]
  64. Nakahata T., Gross A. J., Ogawa M. A stochastic model of self-renewal and commitment to differentiation of the primitive hemopoietic stem cells in culture. J Cell Physiol. 1982 Dec;113(3):455–458. doi: 10.1002/jcp.1041130314. [DOI] [PubMed] [Google Scholar]
  65. Nakahata T., Ogawa M. Identification in culture of a class of hemopoietic colony-forming units with extensive capability to self-renew and generate multipotential hemopoietic colonies. Proc Natl Acad Sci U S A. 1982 Jun;79(12):3843–3847. doi: 10.1073/pnas.79.12.3843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Nicola N. A., Metcalf D., Matsumoto M., Johnson G. R. Purification of a factor inducing differentiation in murine myelomonocytic leukemia cells. Identification as granulocyte colony-stimulating factor. J Biol Chem. 1983 Jul 25;258(14):9017–9023. [PubMed] [Google Scholar]
  67. Nienhuis A. W., Donahue R. E., Karlsson S., Clark S. C., Agricola B., Antinoff N., Pierce J. E., Turner P., Anderson W. F., Nathan D. G. Recombinant human granulocyte-macrophage colony-stimulating factor (GM-CSF) shortens the period of neutropenia after autologous bone marrow transplantation in a primate model. J Clin Invest. 1987 Aug;80(2):573–577. doi: 10.1172/JCI113106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Ogawa M., Porter P. N., Nakahata T. Renewal and commitment to differentiation of hemopoietic stem cells (an interpretive review). Blood. 1983 May;61(5):823–829. [PubMed] [Google Scholar]
  69. Ouellette P. L., Monette F. C. Erythroid progenitors forming clusters in vitro demonstrate high erythropoietin sensitivity. J Cell Physiol. 1980 Oct;105(1):181–184. doi: 10.1002/jcp.1041050119. [DOI] [PubMed] [Google Scholar]
  70. Peschel C., Paul W. E., Ohara J., Green I. Effects of B cell stimulatory factor-1/interleukin 4 on hematopoietic progenitor cells. Blood. 1987 Jul;70(1):254–263. [PubMed] [Google Scholar]
  71. Pharr P. N., Nedelman J., Downs H. P., Ogawa M., Gross A. J. A stochastic model for mast cell proliferation in culture. J Cell Physiol. 1985 Dec;125(3):379–386. doi: 10.1002/jcp.1041250304. [DOI] [PubMed] [Google Scholar]
  72. Razin E., Rifkind A. B., Cordon-Cardo C., Good R. A. Selective growth of a population of human basophil cells in vitro. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5793–5796. doi: 10.1073/pnas.78.9.5793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Rennick D. M., Lee F. D., Yokota T., Arai K. I., Cantor H., Nabel G. J. A cloned MCGF cDNA encodes a multilineage hematopoietic growth factor: multiple activities of interleukin 3. J Immunol. 1985 Feb;134(2):910–914. [PubMed] [Google Scholar]
  74. Rennick D., Yang G., Gemmell L., Lee F. Control of hemopoiesis by a bone marrow stromal cell clone: lipopolysaccharide- and interleukin-1-inducible production of colony-stimulating factors. Blood. 1987 Feb;69(2):682–691. [PubMed] [Google Scholar]
  75. Rennick D., Yang G., Muller-Sieburg C., Smith C., Arai N., Takabe Y., Gemmell L. Interleukin 4 (B-cell stimulatory factor 1) can enhance or antagonize the factor-dependent growth of hemopoietic progenitor cells. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6889–6893. doi: 10.1073/pnas.84.19.6889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Sanderson C. J., O'Garra A., Warren D. J., Klaus G. G. Eosinophil differentiation factor also has B-cell growth factor activity: proposed name interleukin 4. Proc Natl Acad Sci U S A. 1986 Jan;83(2):437–440. doi: 10.1073/pnas.83.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Schrader J. W., Lewis S. J., Clark-Lewis I., Culvenor J. G. The persisting (P) cell: histamine content, regulation by a T cell-derived factor, origin from a bone marrow precursor, and relationship to mast cells. Proc Natl Acad Sci U S A. 1981 Jan;78(1):323–327. doi: 10.1073/pnas.78.1.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Shimamura M., Kobayashi Y., Yuo A., Urabe A., Okabe T., Komatsu Y., Itoh S., Takaku F. Effect of human recombinant granulocyte colony-stimulating factor on hematopoietic injury in mice induced by 5-fluorouracil. Blood. 1987 Jan;69(1):353–355. [PubMed] [Google Scholar]
  79. Sieff C. A., Emerson S. G., Donahue R. E., Nathan D. G., Wang E. A., Wong G. G., Clark S. C. Human recombinant granulocyte-macrophage colony-stimulating factor: a multilineage hematopoietin. Science. 1985 Dec 6;230(4730):1171–1173. doi: 10.1126/science.3877981. [DOI] [PubMed] [Google Scholar]
  80. Sieff C. A., Tsai S., Faller D. V. Interleukin 1 induces cultured human endothelial cell production of granulocyte-macrophage colony-stimulating factor. J Clin Invest. 1987 Jan;79(1):48–51. doi: 10.1172/JCI112806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Sonoda Y., Yang Y. C., Wong G. G., Clark S. C., Ogawa M. Analysis in serum-free culture of the targets of recombinant human hemopoietic growth factors: interleukin 3 and granulocyte/macrophage-colony-stimulating factor are specific for early developmental stages. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4360–4364. doi: 10.1073/pnas.85.12.4360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Stanley E. R., Bartocci A., Patinkin D., Rosendaal M., Bradley T. R. Regulation of very primitive, multipotent, hemopoietic cells by hemopoietin-1. Cell. 1986 Jun 6;45(5):667–674. doi: 10.1016/0092-8674(86)90781-6. [DOI] [PubMed] [Google Scholar]
  83. Stanley E. R., Heard P. M. Factors regulating macrophage production and growth. Purification and some properties of the colony stimulating factor from medium conditioned by mouse L cells. J Biol Chem. 1977 Jun 25;252(12):4305–4312. [PubMed] [Google Scholar]
  84. Suda J., Suda T., Ogawa M. Analysis of differentiation of mouse hemopoietic stem cells in culture by sequential replating of paired progenitors. Blood. 1984 Aug;64(2):393–399. [PubMed] [Google Scholar]
  85. Suda T., Suda J., Ogawa M. Disparate differentiation in mouse hemopoietic colonies derived from paired progenitors. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2520–2524. doi: 10.1073/pnas.81.8.2520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Suda T., Suda J., Ogawa M., Ihle J. N. Permissive role of interleukin 3 (IL-3) in proliferation and differentiation of multipotential hemopoietic progenitors in culture. J Cell Physiol. 1985 Aug;124(2):182–190. doi: 10.1002/jcp.1041240203. [DOI] [PubMed] [Google Scholar]
  87. Suda T., Suda J., Ogawa M. Proliferative kinetics and differentiation of murine blast cell colonies in culture: evidence for variable G0 periods and constant doubling rates of early pluripotent hemopoietic progenitors. J Cell Physiol. 1983 Dec;117(3):308–318. doi: 10.1002/jcp.1041170305. [DOI] [PubMed] [Google Scholar]
  88. Suda T., Suda J., Ogawa M. Single-cell origin of mouse hemopoietic colonies expressing multiple lineages in variable combinations. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6689–6693. doi: 10.1073/pnas.80.21.6689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. TILL J. E., MCCULLOCH E. A., SIMINOVITCH L. A STOCHASTIC MODEL OF STEM CELL PROLIFERATION, BASED ON THE GROWTH OF SPLEEN COLONY-FORMING CELLS. Proc Natl Acad Sci U S A. 1964 Jan;51:29–36. doi: 10.1073/pnas.51.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. TILL J. E., McCULLOCH E. A. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961 Feb;14:213–222. [PubMed] [Google Scholar]
  91. Tayrien G., Rosenberg R. D. Purification and properties of a megakaryocyte stimulatory factor present both in the serum-free conditioned medium of human embryonic kidney cells and in thrombocytopenic plasma. J Biol Chem. 1987 Mar 5;262(7):3262–3268. [PubMed] [Google Scholar]
  92. Tertian G., Yung Y. P., Guy-Grand D., Moore M. A. Long-term in vitro culture of murine mast cells. I. Description of a growth factor-dependent culture technique. J Immunol. 1981 Aug;127(2):788–794. [PubMed] [Google Scholar]
  93. Van Zant G., Goldwasser E. Simultaneous effects of erythropoietin and colony-stimulating factor on bone marrow cells. Science. 1977 Nov 18;198(4318):733–735. doi: 10.1126/science.302986. [DOI] [PubMed] [Google Scholar]
  94. Welte K., Bonilla M. A., Gillio A. P., Boone T. C., Potter G. K., Gabrilove J. L., Moore M. A., O'Reilly R. J., Souza L. M. Recombinant human granulocyte colony-stimulating factor. Effects on hematopoiesis in normal and cyclophosphamide-treated primates. J Exp Med. 1987 Apr 1;165(4):941–948. doi: 10.1084/jem.165.4.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Welte K., Platzer E., Lu L., Gabrilove J. L., Levi E., Mertelsmann R., Moore M. A. Purification and biochemical characterization of human pluripotent hematopoietic colony-stimulating factor. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1526–1530. doi: 10.1073/pnas.82.5.1526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Wong G. G., Witek J. S., Temple P. A., Wilkens K. M., Leary A. C., Luxenberg D. P., Jones S. S., Brown E. L., Kay R. M., Orr E. C. Human GM-CSF: molecular cloning of the complementary DNA and purification of the natural and recombinant proteins. Science. 1985 May 17;228(4701):810–815. doi: 10.1126/science.3923623. [DOI] [PubMed] [Google Scholar]
  97. Wu A. M. Regulation of self-renewal of human T lymphocyte colony-forming units (TL-CFUs). J Cell Physiol. 1983 Oct;117(1):101–108. doi: 10.1002/jcp.1041170114. [DOI] [PubMed] [Google Scholar]
  98. Yang Y. C., Tsai S., Wong G. G., Clark S. C. Interleukin-1 regulation of hematopoietic growth factor production by human stromal fibroblasts. J Cell Physiol. 1988 Feb;134(2):292–296. doi: 10.1002/jcp.1041340217. [DOI] [PubMed] [Google Scholar]
  99. Yokota T., Lee F., Rennick D., Hall C., Arai N., Mosmann T., Nabel G., Cantor H., Arai K. Isolation and characterization of a mouse cDNA clone that expresses mast-cell growth-factor activity in monkey cells. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1070–1074. doi: 10.1073/pnas.81.4.1070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Zilberstein A., Ruggieri R., Korn J. H., Revel M. Structure and expression of cDNA and genes for human interferon-beta-2, a distinct species inducible by growth-stimulatory cytokines. EMBO J. 1986 Oct;5(10):2529–2537. doi: 10.1002/j.1460-2075.1986.tb04531.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Zucali J. R., Dinarello C. A., Oblon D. J., Gross M. A., Anderson L., Weiner R. S. Interleukin 1 stimulates fibroblasts to produce granulocyte-macrophage colony-stimulating activity and prostaglandin E2. J Clin Invest. 1986 Jun;77(6):1857–1863. doi: 10.1172/JCI112512. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Environmental Health Perspectives are provided here courtesy of National Institute of Environmental Health Sciences

RESOURCES