Effect of recombinant interleukin-6 and thrombopoietin on isolated guinea pig bone marrow megakaryocyte protein phosphorylation and proplatelet formation

Blood Cells, Molecules and Diseases

Volumn 23, Issue 2, 1997, Pages 252-268

  Leven, Robert M ^a   Clark, Barbara ^a   Tablin, Fern ^b  

^a RUSH MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Growth factors; Megakaryocytopoiesis; Platelet formation; Signal transduction; Thrombopoietin

Indexed keywords

CALYCULIN A; CYCLIC AMP; GENISTEIN; ISOBUTYLMETHYLXANTHINE; MITOGEN ACTIVATED PROTEIN KINASE; OKADAIC ACID; PHOSPHODIESTERASE INHIBITOR; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; RECOMBINANT INTERLEUKIN 1; RECOMBINANT INTERLEUKIN 3; RECOMBINANT INTERLEUKIN 6; RECOMBINANT THROMBOPOIETIN;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DNA SYNTHESIS; DOSE RESPONSE; DRUG EFFECT; GUINEA PIG; MALE; MEGAKARYOCYTE; MEGAKARYOPOIESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALIA; CAVIA PORCELLUS; SUS SCROFA;

EID: 0031213999     PISSN: 10799796     EISSN: None     Source Type: Journal    
DOI: 10.1006/bcmd.1997.0142     Document Type: Article

References (87)

1. 1. Schulman I, Peirce M, Lukens A, Currimbhoy Z. Studies on thrombopoiesis. I. A factor in normal human plasma required for platelet production; chronic thrombocytopenia due to its deficiency. Blood 16:943-957, 1960.
2. 75selenomethionine. J Clin Invest 48:1615-1626, 1969.
3. 3. Shreiner DP, Levin J. Detection of thrombopoietic activity in plasma by stimulation of suppressed thrombopoiesis. J Clin Invest 49:1709-1713, 1970.
4. 4. Odell Jr. TT, McDonald TP, Asano M: Response of rat megakaryocytes and platelets to bleeding. Acta Haematol 27: 171-179, 1962.
5. 5. Ebbe S, Stohlman F Jr, Overcash J, Donovan J, Howard D. Megakaryocyte size in thrombocytopenic and normal rats. Blood 32:383-392, 1968.
6. 6. Ebbe S, Stohlman F Jr, Donovan J, Overcash J. Megakaryocyte maturation rate in thrombocytopenic rats. Blood 32:787-795, 1968
7. 7. Harker LA. Regulation of thrombopoiesis. Am J Physiol 218:1376-1380, 1970.
8. 8. Pennington DG, Olsen TE. Megakaryocytes in states of altered platelet production: Cell numbers, size and DNA content. Br J Haematol 18:447-463, 1970.
9. 9. MacPherson GG. Changes in megakaryocyte development following thrombocytopenia. Br J Haematol 26:105-115, 1974.
10. 10. Odell TT, JR Murphy, Jackson CW. Stimulation of megakaryocytopoiesis by acute thrombocytopenia in rats. Blood 48:765-775, 1976.
11. 11. Levin J, Bessman JD. The inverse relation between platelet volume and platelet number. Abnormalities in hematologic disease and evidence that platelet size does not correlate with platelet age. J Lab Clin Med 101:295-307, 1983.
12. 12. Ebbe S, T Yee, D Carpenter, Phalen E. Megakaryocytes increase in size within ploidy groups in response to the stimulus of thrombocytopenia. Exp Hematol 16:55-61, 1988.
13. 13. Mayer P, Geissler K, Ward M, Metcalf D. Recombinant human leukemia inhibitory factor induces acute phase proteins and raises the blood platelet counts in nonhuman primates. Blood 81:3226-3233, 1993.
14. 14. Debili N, Masse JM, Katz A, Guichard J, Breton-Gorius J, Vainchenker W. Effects of the recombinant hematopoietic growth factors interleukin-3, interleukin-6, stem cell factor, and leukemia inhibitory factor on the megakaryocytic differentiation of CD34+ cells. Blood 82:84-95, 1993.
15. 15. Tanaka R, Koike K, Imai T, et al. Stem cell factor enhances proliferation, but not maturation, of murine megakaryocytic progenitors in serum-free culture. Blood 80:1743-1749, 1992.
16. 16. Geissler LK, Valent P, Bettelheim P, et al. In vivo synergism of recombinant interleukin-3 and recombinant interleukin-6 on thrombopoiesis in primates. Blood 79:1155-1160, 1992.
17. 17. Stahl CP, Zucker-Franklin D, Evatt BL, Winton EF. Effects of human interleukin-6 on megakaryocyte development and thrombocytopoiesis in primates. Blood 18:1461-1415, 1991.
18. 18. Carrington PA, Hill RJ, Stenberg PE, et al. Multiple in vivo effects of interleukin-3 and interleukin-6 on murine megakaryocytopoiesis. Blood 77:34-41, 1991.
19. 19. Navarro S, Debili N, LeCouedic JP, et al. Interleukin-6 and its receptor are expressed by human megakaryocytes: in vitro effects on proliferation and endoreplication. Blood 77:461-471, 1991.
20. 20. Inoue H, Ishii H, Tsutsumi M, et al. Growth factor-induced process formation of megakaryocytes derived from CFU-MK. Br J Haematol 85:260-269, 1993.
21. 21. Yonemura Y, Kawakita M, Masuda T, Fukimoto K, Takatsuki K. Effect of recombinant human interleukin-11 on rat megakaryopoiesis and thrombopoiesis in vivo: comparative study with interleukin-6. Br J Haematol 84:16-23, 1993.
22. 22. Han ZC, Bellucci S, Wan HY, Caen JP. New insights into the regulation of megakaryocytopoiesis by haematopoietic and fibroblastic growth factors and transforming growth factor beta 1. Br J Haematol 81:1-5, 1992.
23. 23. An E, Ogata K, Kuriya S, Nomura T. Interleukin-6 and erythropoietin act as direct potentiators and inducers of in vitro cytoplasmic process formation on purified mouse megakaryocytes. Exp Hematol 22:149-156, 1994.
24. 24. Ishibashi T, Shikama Y, Kimura H, et al. Thrombopoietic effects of interleukin-6 in long-term administration in mice. Exp Hematol 21:640-646, 1993.
25. 25. Ishida Y, Yano S, Yoshida T, et al. Biological effects of recombinanat erythropoietin, granulocyte-macrophage colony-stimulating factor, interleukin 3, and interleukin 6 on purified rat megakaryocytes. Exp Hematol 19:608-612, 1991.
26. 26. Burstein SA, Mei RL, Henthorn J, Friese P, Turner K. Leukemia inhibitory factor and interleukin-11 promote maturation of murine and human megakaryocytes in vitro. J Cell Physiol 153:305-312, 1992.
27. 27. Broudy VC, Lin NL, Kaushansky K. Thrombopoietin (c-mpl ligand) acts synergistically with erythropoietin, stem cell factor, and interleukin-11 to enhance murine megakaryocyte colony growth and increases megakaryocyte ploidy in vitro. Blood 85:1719-1726, 1995.
28. 28. Hangoc G, Yin T, Cooper S, Schendel P, Yang YC, Broxmeyer HE. In vivo effects of recombinanat interleukin-11 on myelopoiesis in mice. Blood 81: 965-972, 1993.
29. 29. Neben TY, Loebelenz J, Hayes L, et al. Recombinant human interleukin-11 stimulates megakaryocyto-poiesis and increases peripheral platelets in normal and splenectomized mice. Blood 81:901-908, 1993.
30. 30. Nash RA, Seidel KI, Storb R, et al. Effects of rhIL-11 on normal dogs and after sublethal radiation. Exp Hematol 23:389-396, 1995.
31. 31. Zeigler FC, de Sauvage F, Widmer HR, et al. In vitro megakaryocytopoietic and thrombopoietic activity of c-mpl ligand (TPO) on purified murine hematopoietic stem cells. Blood 84:4045-4052, 1994.
32. 32. Imai T, Nakahata T. Stem cell factor promotes proliferation of human primitive megakaryocytic progenitors, but not megakaryocytic maturation. Int J Hematol 59:91-98, 1994.
33. 33. Avraham H, Banu N, Scadden DT, Abraham J, Groopman JE. Modulation of megakaryocytopoiesis by human basic fibroblast growth factor. Blood 83:2126-2132, 1994.
34. 34. Metcalf D, Hilton D, Nicola NA. Leukemia inhibitory factor can potentiate murine megakaryocyte production in vitro. Blood 77:2150-2153, 1991.
35. 35. Debili N, Hegyi E, Navarro S, et al. In vitro effects of hematopoietic growth factors on the proliferation, endoreplication, and maturation of human megakaryocytes. Blood 77:2326-2338, 1991.
36. 36. Kavnoudias H, Jackson H, Ettlinger K, Bertoncello I, McNiece I, Williams N. Interleukin 3 directly stimulates both megakaryocyte progenitor cells and immature megakaryocytes. Exp Hematol 20:43-46, 1992.
37. 37. Monroy RL, Davis TA, Donahue RE, MacVittie TJ. In vivo stimulation of platelet production in a primate model using IL-1 and IL-3. Exp Hematol 19:629-635, 1991.
38. 38. Briddell RA, Brandt JE, Leemhuis TB, Huffman R. Role of cytokines in sustaining long-term human megakaryocytopoiesis in vitro. Blood 79:332-337, 1992.
39. 39. Lok S, Kaushansky K, Holly RD, et al. Cloning and expression of murine thrombopoietin cDNA and stimulation of platelet production in vivo. Nature 369:565-568, 1994.
40. 40. Kaushansky D, Lok S, Holly RD, et al. Promotion of megakaryocyte progenitor expansion and differentiation by the c-Mpl ligand thrombopoietin. Nature 369:568-571, 1994
41. 41. Wendung R, Maraskovsky E, Debili N, et al. c-Mpl ligand is a humoral regulator of megakaryocytopoiesis. Nature 369:571-574, 1994.
42. 42. de Sauvage FJ, Hass PE, Spencer SD, et al. Stimulation of megakarycytopoiesis and thrombopoiesis by the c-Mpl ligand, Nature 369:533-538, 1994.
43. 43. Bartley TD, Bogenberger J, Hunt P, et al. Identification and cloning of a megakaryocyte growth and development factor that is a ligand for the cytokine receptor Mpl. Cell 77:1117-1124, 1994.
44. 44. Methia N, Louache F, Vainchenker W, Wendung F. Oligodeoxynucleotides antisense to the protooncogene c-mpl specifically inhibit in vitro megakaryocytopoiesis. Blood 82:1395-1401, 1993.
45. 45. Gurney AL, Carver-Moore K, de Sauvage FJ, Moore MW. Thrombocytopenia in c-mpl-deficient mice. Science 265:1445-1447, 1994.
46. 46. Guerrero R, Testa U, Gavvianelli M, et al. Unilineage megakaryocytic proliferation and differentiation of purified hematopoietic progenitors in serum-free liquid culture. Blood 86: 3725-3736, 1995.
47. 47. Farese AM, Hunt P, Boone T, MacVittie TJ. Recombinant human megakaryocyte growth and development factor stimulates thrombocytopoiesis in normal nonhuman primates. Blood 86:54-59, 1995.
48. 48. Debili N, Wendung F, Katz A, et al. The mpl-ligand or thrombopoietin or megakaryocyte growth and differentiative factor has both direct proliferative and differentiative activities on human megakaryocyte progenitors. Blood 86:2516-2525, 1995.
49. 49. Angchaisuksiri P, Carlson PL, Dessypris EN. Effects of recombinant human thrombopoietin on megakaryocyte colony and megakaryocyte ploidy by human CD34+ cells in a serum free system. Br J Haematol 93:13-17, 1996.
50. 50. Harker LA, Hunt P, Marza UM, et al. Regulation of platelet production and function by megakaryocyte growth and development factor in nonhumans. Blood 87:33-44, 1996.
51. 51. Nichol JL, Hokom MM, Hornkohl A, et al. Megakaryocyte growth and development factor. Analysis of in vitro effects on human megakaryopoiesis and endogenous serum levels during chemotherapy-induced thrombocytopenia. J Clin Invest 95:2973-2978, 1995.
52. 52. Albrecht M. Studien zur Thrombocytenbildung an Megakaryocyten in menschlichen knochenmarkkulteren. Acta Haematol 17:160-168, 1957.
53. 53. Thiery JP, Bess M. Mecanisme de la plaquettogenese. Rev Hematol 2:167-174, 1956.
54. 54. Izak G, Nelken D, Gurevitch J. Studies on thrombopoiesis.1 II Thrombocytopoiesis in vitro: Experiments with animal and normal human material. Blood 12:507, 1957.
55. 55. Levine RF. Culture in vitro of isolated guinea pig megakaryocytes: Recovery, survival, morphologic changes and maturation. Blood 50:713-725, 1977.
56. 56. Leven RM, Yee MK. Megakaryocyte morphogenesis stimulated in vitro by whole and partially fractionated thrombocytopenic plasma: A model system for the study of platelet formation. Blood 69:1046-1052, 1987.
57. 57. Radley JM, Scurfield G. The mechanism of platelet release. Blood 56:996, 1980.
58. 58. Leven RM. Megakaryocyte motility and platelet formation. Scanning Microscopy 1:1701-1709, 1987.
59. 59. Tablin F, Castro M, Leven RM: Blood platelet formation in vitro: The effects of extracellular matrix and cytoskeleton on megakaryocyte fragmentation. J Cell Sci 97:59-71, 1990.
60. 60. Choi ES, Nichol JL, Hokom MM, Hornkohl AC, Hunt P. Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional. Blood 85:402-413, 1995.
61. 61. Sasaki K, Odai H, Hanazono Y, et al. TPO/c-mpl ligand induces tyrosine phosphorylation of multiple cellular proteins including proto-oncogene products, Vav and c-Cbo, and Ras signaling molecules. Biochem Biophys Res Comm 216:338-347, 1995.
62. 62. Bacon CM, Tortolani PJ, Shimosaka A, Rees RC, Longo DL, O'Shea JJ. Thrombopoietin (TPO) induces tyrosine phosphorylation and activation of STAT5 and STAT3. FEBS Lett 370:63-68, 1995
63. 63. Yamada M, Komatsu N, Okada K, Kato T, Miyazaki H, Miura Y Thrombopoietin induces tyrosine phos-phorylation and activation of mitogen-activated protein kinases in a human thrombopoietin-dependent cell line. Biochem Biophys Res Comm 217:230-237, 1995.
64. 64. Miyakawa Y, Oda A, Druker BJ, et al. Recombinant thrombopoietin induces rapid protein tyrosine phosphorylation of Janus kinase 2 and Shc in human blood platelets. Blood 86:23-27, 1995.
65. 65. Mu SX, Xia M, Elliott G, et al. Megakaryocyte growth and development factor and interleukin-3 induce patterns of protein-tyrosine phosphorylation that correlate with dominant differentiation over proliferation of mpl-transfected 32D cells. Blood 86:4532-4543, 1995.
66. 66. Sattler M, Durstin MA, Frank DA, et al. The thrombopoietin receptor c-MPL activates JAK2 and TYK2 tyrosine kinases. Exp Hematol 23:1040-1048, 1995.
67. 67. Nagata Y, Todokoro K. Thrombopoietin induces activation of at least two distinct signaling pathways. FEBS Lett 377:497-501, 1995
68. 68. Leven RM, Rodriguez A. Immunomagnetic bead isolation of megakaryocytes from guinea-pig bone marrow: effect of recombinant interleukin-6 on size, ploidy and cytoplasmic fragmentation. Br J Haematol 77:267-273, 1991.
69. 69. Laemmli UK. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680-685, 1970.
70. 70. Leven RM. Differential regulation of integrin-mediated proplatelet formation and megakaryocyte spreading. J Cell Physiol 163:597-607, 1995.
71. 71. Hamaguchi H, Takano N, Saito K, Enokihara H, Furusawa S, Shishido H. Interation of monocytes and T cells in the regulation of normal human megakaryocytopoiesis in vitro: role of IL-1 and IL-2. Br J Haematol 76:12-20, 1990.
72. 72. Mazur EM, Cohen JL, Bogart L, et al. Recombinant gibbon interleukin-3 stimulates megakaryocyte colony growth in vitro from human peripheral blood progenitor cells. J Cell Physiol 136:439-677, 1988.
73. 73. Teramura M, Katahira J, Hoshino S, Motoji T, Oshimi K, Mizoguchi H. Clonal growth of human megakaryocyte progenitors in serum-free cultures: Effect of recombinant human interleukin 3. Exp Hematol 16:843-848, 1988.
74. 74. Bruno E, Miller ME, Hoffman R. Interacting cytokines regulate in vitro human megakaryocytopoiesis. Blood 73:671-677, 1989.
75. 75. Matsuda T, Yamanaka Y, Hirano T. Interleukin-6-induced tyrosine phosphorylation of multiple proteins in murine hematopoietic lineage cells. Biochem Biophys Res Comm 200:821-828, 1994.
76. 76. Lutticken C, Coffer P, Yuan J, et al. Interleukin-6-induced serine phosphorylation of transcription factor APRF: evidence for a role in interleukin-6 target gene induction. FEBS Lett 360:137-143, 1995.
77. 77. Matsuda T, Takahashi-Tesuka M, Fukada T, et al. Association and activation of Btk and Tec tyrosine kinases by gp130, a signal transducer of the interleukin-6 family of cytokines. Blood 85:627-633, 1995.
78. 78. Matsuda T, Hirano T. Association of p72 tyrosine kinase with Stat factors and its activation by interleukin-3, interleukin-6, and granulocyte colony-stimulating factor. Blood 83:3457-3461, 1994.
79. 79. Guschin D, Rogers N, Briscoe J, et al. A motor role for the protein tyrosine kinase JAK1 in the JAK/ STAT signal transduction pathway in response to interleukin-6. EMBO J 14:1421-1429, 1995.
80. 80. Yin T, Yang YC. Mitogen-activated protein kinases and ribosomal S6 protein kinases are involved in signaling pathways shared by interleukin-11, interleukin-6, leukemia inhibitory factor, and oncostatin M in mouse 3T3-L1 cells. J Biol Chem 269:3731-3738, 1994
81. 81. Boulton TG, Stahl N, Yancopoulos GD. Ciliary neurotrophic factor/leukemia inhibitory factor/ interleukin 6/oncostatin M family of cytokines induces tyrosine phosphorylation of a common set of proteins overlapping those induced by other cytokines and growth factors. J Biol Chem 269: 11648-11655, 1994.
82. 82. Kumar G, Gupta S, Wang S, Nel AE. Involvement of Janus kinases, p52shc, Raf-1, and MEK-1 in the IL-6-induced mitogen-activated protein kinase cascade of a growth-responsive B cell line. J Immunol 153:4436-4447, 1994.
83. 83. Wang Y, Fuller GM. Phosphorylation and internalization of gp130 occur after IL-6 activation of Jak2 kinase in hepatocytes. Mol Biol Cell 5:819-828, 1994.
84. 84. Wu MP, Jay D, Stracher A. Existence of multiple phosphorylated forms of human platelet actin binding proteins. Cell Mol Biol Res 40:351-357, 1994.
85. 85. Ozawa K, Kashiwada K, Takahashi M, Sobue K. Translocation of cortactin (p80/85)to the actin-based cytoskeleton during thrombin receptor-mediated platelet activation. Exp Cell Res 221:197-204, 1995.
86. 86. Butt E, Abel K, Krieger M, et al. cAMP-and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets. J Biol Chem 269:14509-14517, 1994.
87. 87. Vostal JG, Shulman NR. Vinculin is a major platelet protein that undergoes Ca(2+)-dependent tyrosine phosphorylation. Biochem J 294:675-680, 1993.