89
Views
14
CrossRef citations to date
0
Altmetric
Original Article

ALL-Trans Retinoic Acid and Hematopoietic Growth Factors Regulating the Growth and Differentiation of Blast Progenitors in Acute Promyelocytic Leukemia

Pages 267-280 | Accepted 16 Jun 1998, Published online: 01 Jul 2009

References

  • Bennett J. M., Catovsky D., Daniel M. T., Flandrin G., Galton D. A. G., Gralnick H. R., Sultan C. Proposals for the classification of the acute leukaemias. British Journal of Haematology 1976; 33: 451–458
  • Bennett J. M., Catovsky D., Daniel M. T., Flandrin G., Galton D. A. G., Gralnick H. R., Sultan C. A variant form of hypergranular promyelocytic leukemia (M3). Annals of Internal Medicine 1980; 92: 261
  • Castaigne S., Chomienne C., Daniel M. T., Ballerini P., Berger R., Fenaux P., Degos L. All‐trans‐retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results. Blood. 1990; 76: 1704–1709
  • Larson R. A., Kondo K., Vardiman J. W., Butler A. E., Golomb H. M., Rowley J. D. Evidence for a 15;17 translocation in every patient with acute promyelocytic leukemia. American Journal of Medicine 1984; 76: 827–841
  • Pandolfi P. P. PML, PLZF and NPM genes in the molecular pathogenesis of acute promyelocytic leukemia. Haematologica 1996; 81: 472–482
  • Huang M., Ye Y., Chen S., Chai J., Lu J. ‐X., Zhoa L., Gu L., Wang Z. Use of all‐trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood 1988; 72: 567–572
  • Chomienne C., Ballerini P., Balitrand N., Amar M., Bernard J. F., Boivin P., Daniel M. T., Berger R., Castaigne S., Degos L. Retinoic acid therapy for promyelocytic leukemia. Lancet 1989; 1: 746
  • Chomienne C., Ballerini P., Balitrand N., Daniel M. T., Fenaux P., Castaigne S., Degos L. All‐trans‐retinoic acid in acute promyelocytic leukemias. II. In vitro studies: Structure‐function relationship. Blood 1990; 76: 1710–1717
  • Warrell R. P., Jr, Frankel S. R., Miller W. H., Jr, Scheinberg D. A., Itri L. M., Hittelman W. N., Vyas R., Andreeff M., Tafuri A., Jakubowski A., Gabrilove J., Gordon M. S., Dmitrovsky E. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all‐trans‐retinoic acid). New England Journal of Medicine 1991; 324: 1385–1393
  • Grignani E., Fagioli M., Alcalay M., Longo L., Pandolfi P. P., Donti E., Biondi A., Lo Coco F., Pelicci P. G. Acute promyelocytic leukemia: From genetics to treatment. Blood 1994; 83: 10–25
  • Degos L., Dombret H., Chomienne C., Daniel M. T., Micléa J. ‐M., Chastang C., Castaigne S., Fenaux P. All‐trans‐retinoic acid as a differentiating agent in the treatment of acute promyelocytic leukemia. Blood 1995; 85: 2643–2653
  • Tallman M. S., Andersen J. W., Schiffer C. A., Appelbaum F. R., Feusner J. H., Ogden A., Shepherd L., Willman C., Bloomfield C. D., Rowe J. M., Wiernik P. H. All‐trans‐retinoic acid in acute promyelocytic leukemia. New England Journal of Medicine 1997; 337: 1021–1028
  • Warrell R. P., Jr., de Thé H., Wang Z. Y., Degos L. Acute promyelocytic leukemia. New England Journal of Medicine 1993; 329: 177–189
  • Sacchi S., Russo D., Awisati G., Dastoli G., Lazzarino M., Pelicci P. G., Bonora R., Visani G., Grassi C., Iacona I., Luzzi L., Vanzanelli P. All‐trans retinoic acid in hematological malignancies. An update. Haematologica 1997; 82: 106–121
  • McCulloch E. A. Stem cells in normal and leukemic hemopoiesis (Henry Stratton Lecture, 1982). Blood 1983; 62: 1–13
  • Griffin J. D., Löwenberg B. Clonogenic cells in acute myeloblastic leukemia. Blood 1986; 68: 1185–1195
  • Miyauchi J. Hematopoietic growth factors and blast progenitors in acute leukemia. Hematology 1998, In Press
  • Bainton D. F. Abnormal neutrophils in acute myelogenous leukemia: Identification of subpopulations based on analysis of azurophil and specific granules. Blood Cells 1975; 1: 191–199
  • Bainton D. F., Friedlander L. M., Shohet S. B. Abnormalities in granule formation in acute myelogenous leukemia. Blood 1977; 49: 693–704
  • Dittman W. A., Kramer R. J., Bainton D. F. Electron microscopic and peroxidae cytochemical analysis of pink pseudo‐Chediak‐Higashi granules in acute myelogenous leukemia. Cancer Research 1980; 40: 4473–4481
  • Miyauchi J., Watanabe Y., Enomoto Y., Takeuchi K. Lactoferrin‐deficient neutrophil polymorphonuclear leucocytes in leukaemias: a semiquantitative and ultrastructural cytochemical study. Journal of Clinical Pathology 1983; 36: 1397–1405
  • Housset M., Daniel M. T., Degos L. Small doses of ARA‐C in the treatment of acute myeloid leukaemia: Differentiation of myeloid leukaemia cells?. British Journal of Haematology 1982; 51: 125–129
  • Castaigne S., Daniel M. T., Herait P., Degos L. Does treatment with ARA‐C in low dosage cause differentiation of leukemic cells?. Blood 1983; 62: 85–86
  • Beran M., Hittelman W. N., Andersson B. S., McCredie K. B. Induction of differentiation in human myeloid leukemia cells with cytosine arabinoside. Leukemia Research 1986; 10: 1033–1039
  • Hittelman W. N., Agbor P., Petkovic I., Andersson B., Kantarjian H., Walters R., Roller C., Beran M. Detection of leukemic clone maturation in vivo by premature chromosome condensation. Blood 1988; 72: 1950–1960
  • Jacobson R. J., Temple M. J., Singer J. W., Raskind W., Powell J., Fialkow P. J. A clonal complete remission in a patient with acute nonlymphocytic leukemia originating in a multipotent stem cell. New England Journal of Medicine 1984; 310: 1513–1517
  • Fialkow P. J., Singer J. W., Raskind W. H., Adamson J. W., Jacobson R. J., Bernstein I. D., Dow L. W., Najfeld V., Veith R. Clonal development, stem‐cell differentiation, and clinical remissions in acute nonlymphocytic leukemia. New England Journal of Medicine 1987; 317: 468–473
  • Fearon E. R., Burke P. J., Schiffer C. A., Zehnbauer B. A., Vogelstein B. Differentiation of leukemia cells to polymorphonuclear leukocytes in patients with acute nonlymphocytic leukemia. New England Journal of Medicine 1986; 315: 15–24
  • Sachs L. Control of normal cell differentiation and the phenotypic reversion of malignancy in myeloid leukaemia. Nature 1978; 274: 535–539
  • Sachs L. Cell differentiation and bypassing of genetic defects in the suppression of malignancy. Cancer Research 1987; 47: 1981–1986
  • Koeffler H. P. Induction of differentiation of human acute myelogenous leukemia cells: Therapeutic implications. Blood 1983; 62: 709–721
  • Honma Y., Kasukabe T., Okabe J., Hozumi M. Prolongation of survival time of mice inoculated with myeloid leukemia cells by inducers of normal differentiation. Cancer Research 1979; 39: 3167–3171
  • Collins S. J. The HL‐60 promyelocytic leukemia cell line: Proliferation, differentiation, and cellular oncogene expression. Blood 1987; 70: 1233–1244
  • Dalton W. T., Jr., Aheam M. J., McCredie K. B., Freireich E. J., Stass S. A., Trujillo J. M. HL‐60 cell line was derived from a patient with FAB‐M2 and not FAB‐M3. Blood 1988; 71: 242–247
  • Fontana J. A., Colbert D. A., Deisseroth A. B. Identification of a population of bipotent stem cells in the HL60 human promyelocytic leukemia cell line. Proceedings of the National Academy of Sciences of the United States of America 1981; 78: 3863–3866
  • Collins S. J., Ruscetti F. W., Gallagher R. E., Gallo R. C. Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proceedings of the National Academy of Sciences of the United States of America 1978; 75: 2458–2462
  • Newburger P. E., Chovaniec M. E., Greenberger J. S., Cohen H. J. Functional changes in human leukemic cell line HL‐60. Journal of Cell Biology 1979; 82: 315–322
  • Collins S. J., Ruscetti F. W., Gallagher R. E., Gallo R. C. Normal functional characteristics of cultured human promyelocytic leukemia cells (HL‐60) after induction of differentiation by dimethylsulfoxide. Journal of Experimental Medicine 1979; 149: 969–974
  • Breitman T. R., Selonick S. E., Collins S. J. Induction of differentiation of the human promyelocytic leukemia cell line (HL‐60) by retinoic acid. Proceedings of the National Academy of Sciences of the United States of America 1980; 77: 2936–2940
  • Tobler A., Dawson M. I., Koeffler H. P. Retinoids: Structure‐function relationship in normal and leukemic hematopoiesis in vitro. Journal of Clinical Investigation 1986; 78: 303–309
  • Imaizumi M., Breitman T. R. Retinoic acid‐induced differentiation of the human promyelocytic leukemia cell line, HL‐60, and fresh human leukemia cells in primary culture: A model for differentiation inducing therapy of leukemia. European Journal of Haematology 1987; 38: 289–302
  • Tanaka H., Abe E., Miyaura C., Shiina Y., Suda T. 1 alpha, 25‐dihydroxyvitamin D3 induces differentiation of human promyelocytic leukemia cells (HL‐60) into monocyte‐macrophages, but not into granulocytes. Biochemical and Biophysical Research Communications 1983; 117: 86–92
  • McCarthy D. M., San‐Miguel J. F., Freake H. C., Green P. M., Zola H., Catovsky D., Goldman J. M. 1,25‐dihydroxyvitamin D3 inhibits proliferation of human promyelocytic leukaemia (HL60) cells and induces monocyte‐macrophage differentiation in HL60 and normal human bone marrow cells. Leukemia Research 1983; 7: 51–55
  • Rovera G., O'Brien T. G., Diamond L. Induction of differentiation in human promyelocytic leukemia cells by tumor promoters. Science 1979; 204: 868–870
  • Rovera G., Santoli D., Damsky C. Human promyelocytic leukemia cells in culture differentiate into mac‐rophage‐like cells when treated with a phorbol diester. Proceedings of the National Academy of Sciences of the United States of America 1979; 76: 2779–2783
  • Giguère V. Retinoic acid receptors and cellular retinoid binding proteins: Complex interplay in retinoid signaling. Endocrine Reviews 1994; 15: 61–79
  • De Luca L. M. Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB Journal 1991; 5: 2924–2933
  • Breitman T. R., Collins S. J., Keene B. R. Terminal differentiation of human promyelocytic leukemic cells in primary culture in response to retinoic acid. Blood 1981; 57: 1000–1004
  • Flynn P. J., Miller W. J., Weisdorf D. J., Arthur D. C., Brunning R., Branda R. F. Retinoic acid treatment of acute promyelocytic leukemia: In vitro and in vivo observations. Blood 1983; 62: 1211–1217
  • Nilsson B. Probable in vivo induction of differentiation by retinoic acid of promyelocytes in acute promyelocytic leukaemia. British Journal of Haematology 1984; 57: 365–371
  • Fontana J. A., Rogers J. S., Durham J. P. The role of 13 cis‐retinoic acid in the remission induction of a patient with acute promyelocytic leukemia. Cancer 1986; 57: 209–217
  • Douer D., Koeffler H. P. Retinoic acid enhances colony‐stimulating factor‐induced clonal growth of normal human myeloid progenitor cells in vitro. Experimental Cell Research 1982; 138: 193–198
  • Douer D., Koeffler H. P. Retinoic acid enhances growth of human early erythroid progenitor cells in vitro. Journal of Clinical Investigation 1982; 69: 1039–1041
  • Bradley E. C., Ruscetti F. W., Steinberg H., Paradise C., Blaine K. Inhibition of differentiation and proliferation of colony‐stimulating factor‐induced clonal growth of normal human marrow cells in vitro by retinoic acid. Journal of the National Cancer Institute 1983; 71: 1189–1192
  • Van Bockstaele D. R., Lenjou M., Snoeck H. ‐W., Lardon F., Stryckmans P., Peetermans M. E. Direct effects of 13‐cis and all‐trans retinoic acid on normal bone marrow (BM) progenitors: Comparative study on BM mononuclear cells and on isolated CD34+ BM cells. Annals of Hematology 1993; 66: 61–66
  • Gratas C., Menot M. L., Dresch C., Chomienne C. Retinic acid supports granulocytic but not erythroid differentiation of myeloid progenitors in normal bone marrow cells. Leukemia 1993; 7: 1156–1162
  • Labbaye C., Valtieri M., Testa U., Giampaolo A., Meccia E., Sterpetti P., Parolini I., Pelosi E., Bulgarini D., Cayre Y. E., Peschle C. Retinoic acid down‐modulates erythroid differentiation and GATA1 expression in purified adult‐progenitor culture. Blood 1994; 83: 651–656
  • Douer D., Koeffler H. P. Retinoic acid: Inhibition of the clonal growth of human myeloid leukemia cells. Journal of Clinical Investigation 1982; 69: 277–283
  • Gallagher R. E., Lurie K. J., Leavitt R. D., Wiernik P. H. Effects of interferon and retinoic acid on the growth and differentiation of clonogenic leukemic cells from acute myelogenous leukemia patients treated with recombinant leukocyte‐αA interferon. Leukemia Research 1987; 11: 609–619
  • Wang C., Curtis J. E., Minden M. D., McCulloch E. A. Expression of a retinoic acid receptor gene in myeloid leukemia cells. Leukemia 1989; 3: 264–269
  • Tohda S., Curtis J. E., McCulloch E. A., Minden M. D. Comparison of the effects of all‐trans and cis‐retinoic acid on the blast stem cells of acute myeloblastic leukemia in culture. Leukemia 1992; 6: 656–661
  • Lawrence H. J., Conner K., Kelly M. A., Haussler M. R., Wallace P., Bagny G. C., Jr. Cis‐retioic acid stimulates the clonal growth of some myeloid leukemia cells in vitro. Blood 1987; 69: 302–307
  • Findley H. W., Jr, Steuber C. P., Ruymann F. B., Culbert S., Ragab A. H. Effect of retinoic acid on the clonal growth of childhood myeloid and lymphoid leukemias: A pediatric oncology group study. Experimental Hematology 1984; 12: 768–773
  • Tohda S., Minden M. D. Modulation of growth factor receptors on acute myeloblastic leukemia cells by retinoic acid. Japanese Journal of Cancer Research 1994; 85: 378–383
  • Tohda S., Minden M. D., McCulloch E. A. Interactions between retinoic acid and colony‐stimulating factors affecting the blast cells of acute myeloblastic leukemia. Leukemia 1991; 5: 951–957
  • Kizaki M., Ikeda Y., Tanosaki R., Nakajima H., Morikawa M., Sakashita A., Koeffler H. P. Effects of novel retinoic acid compound, 9‐cis‐retinoic acid, on proliferation, differentiation, and expression of retinoic acid receptor‐α and retinoid X receptor‐α RNA by HL‐60 cells. Blood 1993; 82: 3592–3599
  • Lanotte M., Martin‐Thouvenin V., Najman S., Balerini P., Valensi F., Berger R. NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood 1991; 77: 1080–1086
  • Miyauchi J., Inatotni Y., Ohyashiki K., Asada M., Mizutani S., Toyama K. The in vitro effects of all‐trans‐retinoic acid and hematopoietic growth factors on the clonal growth and self‐renewal of blast stem cells in acute promyelocytic leukemia. Leukemia Research 1997; 21: 285–294
  • McCulloch E. A., Kelleher C. A., Miyauchi J., Wang C., Cheng G. Y. N., Minden M. D., Curtis J. E. Heterogeneity in acute myeloblastic leukemia. Leukemia 1988; 2: 38S–49S, Suppl
  • Clark S. C., Kamen R. The human hematopoietic colony‐stimulating factors. Science 1987; 236: 1229–1237
  • Pébusque M. J., Lafage M., Lopez M., Mannoni P. Preferential response of acute myeloid leukemias with translocation involving chromosome 17 to human recombinant granulocyte colony‐stimulating factor. Blood 1988; 72: 257–265
  • Vaickus L., Villalona‐Calero M. A., Caligiuri T. Acute progranulocytic leukemia (APL): Possible in vivo differentiation by granulocyte colony‐stimulating factor (G‐CSF). Leukemia 1993; 7: 1680–1681
  • Takamatsu H., Nakao S., Ohtake S., Chuhjo T., Yamaguchi M., Shiobara S., Matsuda T. Granulocyte colony‐stimulating factor‐dependent leukemic cell proliferation in vivo in acute promyelocytic leukemia. Blood 1993; 81: 3485–3486
  • Le Beau M. M., Lemons R. S., Carrino J. J., Pettenati M. J., Souza L. M., Diaz M. O., Rowley J. D. Chromosomal localization of the human G‐CSF gene to 17q11 proximal to the breakpoint of the t(15;17) in acute promyelocytic leukemia. Leukemia 1987; 1: 797–799
  • Simmers R. N., Webber L. M., Shannon M. F., Garson O. M., Wong G., Vadas M. A., Southerland G. R. Localization of the G‐CSF gene on chromosome 17 proximal to the breakpoint in the t(15;17) in acute promyelocytic leukemia. Blood 1987; 70: 330–332
  • Tanaka S., Nishigaki H., Misawa S., Taniwaki M., Nakagawa H., Yashige H., Horiike S., Kashima K., Inazawa J., Sonoda Y., Abe T. Lack of involvement of the G‐CSF gene by chromosomal translocation t(15;17) in acute promyelocytic leukemia. Leukemia 1990; 4: 494–496
  • Gianni M., Terao M., Zanotta S., Barbui T., Rambaldi A., Garattini E. Retinoic acid and granulocyte colony‐stimulating factor synergistically induce leukocyte alkaline phosphatase in acute promyelocytic leukemia cells. Blood 1994; 83: 1909–1921
  • Garattini E., Gianni M. Leukocyte alkaline phosphatase a specific marker for the post‐mitotic neutrophilic granulocyte: Regulation in acute promyelocytic leukemia. Leukemia and Lymphoma 1996; 23: 493–503
  • Nakamaki T., Sakashita A., Sano M., Hino K., Suzuki K., Tomoyasu S., Tsuruoka N., Honma Y., Hozumi M. Granulocyte‐colony stimulating factor and retinoic acid cooperatively induce granulocytic differentiation of acute promyelocytic leukemia cells in vitro. Japanese Journal of Cancer Research 1989; 80: 1077–1082
  • Sakashita A., Nakamaki T., Tsuruoka N., Honma Y., Hozumi M. Granulocyte colony‐stimulating factor, not granulocyte‐macrophage colony‐stimulating factor, co‐operates with retinoic acid on the induction of functional N‐formyl‐methionyl‐phenylalanine receptors in HL‐60 cells. Leukemia 1991; 5: 26–31
  • Imaizumi M., Sato A., Koizumi Y., Inoue S., Suzuki H., Suwabe N., Yoshinari M., Ichinohasama R., Endo K., Sawai T., Tada K. Potentiated maturation with a high proliferating activity of acute promyelocytic leukemia induced in vitro by granulocyte or granulocyte/macrophage colony‐stimulating factors in combination with ail‐trans retinoic acid. Leukemia 1994; 8: 1301–1308
  • Hemmi H., Breitman T. Combination of recombinant human interferons and retinoic acid synergistically induce differetiatiaion of the human promyelocytic leukemia cell line HL‐60. Blood 1987; 69: 501–507
  • Trinchieri G., Rosen M., Perussia B. Retinoic acid cooperates with tumor necrosis factor and immune interferon in inducing differentiation and growth inhibition of the human promyelocytic leukemic cell line HL‐60. Blood 1987; 69: 1218–1224
  • Tobler A., Munker R., Heitjan D., Koeffler H. P. In vitro interaction of recombinant tumor necrosis factor α and all‐trans‐retinoic acid with normal and leukemic hematopoietic cells. Blood 1987; 70: 1940–1946
  • Bollag W. Retinoids and interferon: A new promising combination?. British Journal of Haematology 1991; 79: 87–91
  • Bollag W., Majewski S., Jablonska S. Cancer combination chemotherapy with retinoids: experimental rationale. Leukemia 1994; 8: 1453–1457
  • Olsson I. L., Breitman T. R., Gallo R. C. Priming of human myeloid leukemic cell lines HL‐60 and U‐937 with retinoic acid for differentiation effects of cyclic adenosine 3′:5′‐monophosphate‐inducing agents and a T‐lymphocyte‐derived differentiation factor. Cancer Research 1982; 42: 3928–3933
  • Ruchaud S., Duprez E., Gendron M. C., Houge G., Genieser H. G., Jastorff B., Doskeland S. O., Lanotte M. Two distinctly regulated events, priming and triggering, during retinoid‐induced maturation and resistance of NB4 promyelocytic leukemia cell line. Proceedings of the National Academy of Sciences of the United States of America 1994; 91: 8428–8432
  • Gianni M., Terao M., Norio P., Barbui T., Rambaldi A., Garattini E. All‐trans retinoic acid and cyclic adenosine monophosphate cooperate in the expression of leukocyte alkaline phosphatase in acute promyelocytic leukemia cells. Blood 1995; 85: 3619–3635
  • Chomienne C., Balitrand N., Degos L., Abita J. ‐P. 1‐B‐D arabinofuranosyl cytosine and all‐trans retinoic acid in combination accelerates and increases monocyte differentiation of myeloid leukemic cells. Leukemia Research 1986; 10: 631–636
  • Becker P. S., Li Z., Potselueva T., Madri J. A., Newburger P. E., Berliner N. Laminin promotes differentiation of NB4 promyelocytic leukemia cells with all‐trans retinoic acid. Blood 1996; 88: 261–267
  • Santini V., Colombat Ph., Delwel R., van Gurp R., Touw I., Löwenberg B. Induction of granulocyte maturation in acute myeloid leukemia by G‐CSF and retinoic acid. Leukemia Research 1991; 15: 341–350
  • Colombat Ph., Santini V., Delwel R., Krefft J., Bredmond J. L., Löwenberg B. Primary human acute myeloblastic leukaemia: An analysis of in vitro granulocytic maturation following stimulation with retinoic acid and G‐CSF. British Journal of Haematology 1991; 79: 382–389
  • Li J., Sartorelli A. C. Synergistic induction of the differentiation of WEHI‐3BD+ myelomonocytic leukemia cells by retinoic acid and granulocyte colony‐stimulating factor. Leukemia Research 1992; 16: 571–576
  • Valtieri M., Boccoli G., Testa U., Barletta C., Peschle C. Two‐step differentiation of AML‐193 leukemic line: Terminal maturation is induced by positive interaction of retinoic acid with granulocyte colony‐stimulating factor (CSF) and vitamin D3 with monocyte CSF. Blood 1991; 77: 1804–1812
  • 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., Welte K. Recombinant human granulocyte colony‐stimulating factor: Effects on normal and leukemic myeloid cells. Science 1986; 232: 61–65
  • Matsuda S., Shirafuji N., Asano S. Human granulocyte colony stimulating factor specifically binds to murine myeloblastic NFS‐60 cells and activates their guanosine triphosphate binding proteins/adenylate cyclase system. Blood 1989; 74: 2343–2348
  • McCulloch E. A., Minden M. D., Miyauchi J., Kelleher C. A., Wang C. Stem cell renewal and differentiation in acute myeloblastic leukaemia. Journal of Cell Science. 1988; 10: 267–281, Suppl
  • Dubois C., Schlageter M. H., de Gentile A., Guidez F., Balitrand N., Toubert M. E., Krawice I., Fenaux P., Castaigne S., Najean Y., Degos L., Chomienne C. Hematopoietic growth factor expression and ATRA sensitivity in acute promyelocytic blast cells. Blood 1994; 83: 3264–3270
  • Hassan H. T., Drexler H. G. Interleukins and colony stimulating factors in human myeloid leukemia cell lines. Leukemia and Lymphoma 1995; 20: 1–15
  • de Koning J. P., Soede‐Bobok A. A., Schelen A. M., Smith L., van Leeuwen D., Santini V., Burgering B. M. T., Bos J. L., Löwenberg B., Touw L. P. Proliferation signaling and activation of she, p21ras, and myc via tyrosine 764 of human granulocyte colony‐stimulating factor receptor. Blood 1998; 91: 1924–1933
  • Borregaard N., Cowland J. B. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 1997; 89: 3503–3521
  • Bainton D. F., Ullyot J. L., Farquhar M. G. The development of neutrophil polymorphonuclear leukocytes in human bone marrow. Journal of Experimental Medicine 1971; 134: 907–934
  • Marmont A. M., Damasio E., Zucker‐Franklin D. Neutrophils: Normal structure and physiology. 1. Differentiation and maturation. Atlas of Blood Cells: Function and Pathology2nd edn, D. Zucker‐Franklin, M. E. Greaves, C. E. Grossi, A. M. Marmont. Edi‐Ermes, Milano 1988; 159–246
  • Brederoo P., van der Meulen J., Mommaas Kienhuis A. M. Development of the granule population in neutrophil granulocytes from bone marrow. Cell and Tissue Research 1983; 2324: 469–496
  • Brederoo P., van der Meulen J., Daems W. Ultrastructural localization of peroxidase activity in developing neutrophil granulocytes from human bone marrow. Histochemistry 1986; 84: 445–453
  • Rice W. G., Ganz T., Kinkade J. M., Jr, Selsted M. E., Lehrer R. I., Parmley R. T. Defensin‐rich dense granules of human neutrophils. Blood 1987; 70: 757–765
  • Oren A., Taylor J. M. G. The subcellular localization of defensins and myeloperoxidase in human neutrophilis: Immunocytochemical evidence for azurophil granule heterogeneity. Journal of Laboratory and Clinical Medicine 1995; 125: 340–347
  • Pryzwansky K. B., Breton‐Gorius J. Identification of a subpopulation of primary granules in human neutrophils based upon maturation and distribution: Study by transmission electron microscopy cytochemistry and high voltage electron microscopy of whole cell preparations. Laboratory Investigation 1985; 53: 664–671
  • Parmley R. T., Rice W. G., Kinkade J. M., Jr, Gilbert C., Barton J. C. Peroxidase‐containing microgranules in human neutrophils: Physical, morphological, cytochemical, and secretory properties. Blood 1987; 70: 1630–1638
  • Parmley R. T., Takagi M., Barton J. C., Boxer L. A., Austin R. L. Ultrastructural localization of lactoferrin and iron‐binding protein in human neutrophils and rabbit heterophils. American Journal of Pathology 1982; 109: 343–358
  • Cramer E., Pryzwansky K. B., Villeval J. L., Testa U., Breton‐Gorius J. Ultrastructural localization of lactoferrin and myeloperoxidase in human neutrophils by immunogold. Blood 1985; 65: 423–432
  • Miyauchi J., Watanabe Y. Immunocytochemical localization of lactoferrin in human neutrophils: an ultrastructural and morphometrical study. Cell and Tissue Research 1987; 247: 249–258
  • Hibbs M. S., Bainton D. F. Human neutrophil gelatinase is a component of specific granules. Journal of Clinical Investigation 1989; 84: 1395–1402
  • Kjeldsen L., Bainton D. F., Sengeløv H., Borregaard N. Structural and functional heterogeneity among peroxidase‐negative granules in human neutrophils: Identification of a distinct gelatinase‐containing granule subset by combined immunocytochemistry and subcellular fractionation. Blood 1993; 82: 3183–3191
  • Borregaard N., Sehested M., Nielsen B. S., Sengeløv H., Kjeldsen L. Biosynthesis of granule proteins in normal human bone marrow cells. Gelatinase is a marker of terminal neutrophil differentiation. Blood 1995; 85: 812–817
  • Miyauchi J., Ohyashiki K., Inatomi Y., Toyama K. Neutrophil secondary‐granule deficiency as a hallmark of all‐trans retinoic acid‐induced differentiation of acute promyelocytic leukemia cells. Blood 1997; 90: 803–813
  • Bessis M. Living blood cells and their ultrastructure. Springer‐Verlag, Berlin/Heidelberg/New York 1973
  • Ahearn M. J., Trujillo J. M., Fowler A., Hart J. S. The association of nuclear blebs with aneuploidy in human acute leukemia. Cancer Research 1974; 34: 2887–2896
  • Vyas R. C., Frankel S. R., Agbor P., Miller W. H., Jr, Warrell R. P., Jr., Hittelman W. N. Probing the pathobiology of response to all‐trans retinoic acid in acute promyelocytic leukemia: Premature chromosome condensation/fluorescence in situ hybridization analysis. Blood 1996; 87: 218–226
  • Elliott S., Taylor K., White S., Rodwell R., Marlton P., Meagher D., Wiley J., Taylor D., Wright S., Timms P. Proof of differentiative mode of action of all‐trans retinoic acid in acute promyelocytic leukemia using X‐linked clonal analysis. Blood 1992; 79: 1916–1919
  • Rado T. A., Wei X., Benz E. J., Jr. Isolation of lactoferrin cDNA from a human myeloid library and expression of mRNA during normal and leukemic myelopoiesis. Blood 1987; 70: 989–993
  • Lübbert M., Herrmann F., Koeffler H. P. Expression and regulation of myeloid‐specific genes in normal and leukemic myeloid cells. Blood 1991; 77: 909–924
  • Johnston J. J., Rintels P., Chung J., Sather J., Benz E. J., Jr., Berliner N. Lactoferrin gene promoter: Structural integrity and nonexpression in HL60 cells. Blood 1992; 79: 2998–3006
  • Khanna‐Gupta A., Kolibaba K., Zibello T. A., Berliner N. NB4 cells show bilineage potential and an aberrant pattern of neutrophil secondary granule protein gene expression. Blood 1994; 84: 294–302
  • Parmley R. T., Ogawa M., Darby C. P., Jr., Spicer S. S. Congenital neutropenia: Neutrophil proliferation with abnormal maturation. Blood 1975; 46: 723–734
  • Salmon S. E., Cline M. J., Schultz J., Lehrer R. I. Myeloperoxidase deficiency. New England Journal of Medicine 1976; 282: 250–253
  • Rausch P. G., Pryzwansky K. B., Spitznagel J. K. Immunocytochemical identification of azurophilic and specific granule markers in the giant granules of Chediak‐Higashi neutrophils. New England Journal of Medicine 1978; 298: 693–698
  • Spicer S. S., Sato A., Vincent R., Eguchi M., Poon K. C. Lysosome enlargement in the Chediak‐Higashi syndrome. Federation Proceedings 1981; 40: 1451–1455
  • Schmalzl F., Huhn D., Asamer H., Rindler R., Braunsteiner H. Cytochemistry and ultrastructure of pathologic granulation in myelogenous leukemia. Blut 1973; 27: 243–260
  • Catovsky D., Galton D. A. G., Robinson J. Myeloperoxidase‐deficient neutrophils in acute myeloid leukaemia. Scandinavian Journal of Haematology 1972; 9: 142–148
  • Rausch P. G., Pryzwansky K. B., Spitznagel J. K., Herion J. C. Immunocytochemical identification of abnormal polymorphonuclear neutrophils in patients with leukemia. Blood Cells 1978; 4: 369–376
  • Ullyot J. L., Bainton D. F. Azurophil and specific granules of blood neutrophils in chronic myelogenous leukemia: An ultrastructural and cytochemical analysis. Blood 1974; 44: 469–482
  • Breton‐Gorius J., Houssay D., Dreyfus B. Partial myeloperoxidase deficiency in a case of preleukaemia. British Journal of Haematology 1975; 30: 273–288
  • Breton‐Gorius J., Coquin Y., Vilde J. L., Dreyfus B. Cytochemical and ultrastructural studies of aberrant granules in the neutrophils of two patients with myeloperoxidase deficiency during a preleukemic state. Blood Cells 1976; 2: 187–209
  • Komiyama A., Morosawa H., Nakahata T., Miyagawa Y., Akabane T. Abnormal neutrophil maturation in a neutrophil defect with morphologic abnormality and impaired function. Journal of Pediatrics 1979; 94: 19–25
  • Strauss R. G., Bove K. E., Jones J. F., Mauer A. M., Fulginiti V. A. An anomaly of neutrophil morphology with impaired function. New England Journal of Medicine 1974; 290: 478–484
  • Breton‐Gorius J., Mason D. Y., Buriot D., Vilde J. L., Griscelli C. Lactoferrin deficiency as a consequence of a lack of specific granules in neutrophils from a patient with recurrent infections. American Journal of Pathology 1980; 99: 413–429

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.