Stromal Cells in Long-Term Bone Marrow Cultures

  • Peter J. Quesenberry
Part of the Contemporary Biomedicine book series (CB, volume 9)


The introduction of systems for the growth of long-term liquid culture of murine marrow cells has provided unique opportunities for the study of the role of accessory stromal cells in regulating hemopoiesis.1–3 A number of in vivo observations (reviewed elsewhere in this volume) including those on the selective anatomical localization of different differentiation pathways after marrow transplant, 4–6 the organ distribution of hemopoiesis under stressed conditions (endotoxin, anemia), 7–8 and the stromal deficit in SL/SLd9–10 mice all provided evidence for the existence of an hematopoietic inductive microenvironment. But these in vivo systems did not lend themselves to studies on the specific stromal cells involved in such regulation. Bessis and colleagues11 have provided intriguing morphologic observations indicating that macrophages may act as “nurse cells” for erythroid cells. Weiss and coworkers12–15 and Chamberlin et al.16 have described the adventitial reticular cell (ARC) of the marrow as an interesting candidate stromal cell. This “ARC” abutts the abluminal side of sinusoidal endothelial cells17, 18 and sends processes throughout the marrow sinusoid touching many different cells and providing an obvious means of “networking” among the marrow cell populations.


Stromal Cell Epithelioid Cell Bone Marrow Culture Hemopoietic Stem Cell Hemopoietic Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Dexter, T. M., Allen, T. D., and Lajtha L. G. (1977) J. Cell Physiol. 91, 335–344.PubMedGoogle Scholar
  2. 2.
    Dexter, T. M. and Lajtha, L. G. (1974) Br. J. Haematol. 28, 525–530.PubMedGoogle Scholar
  3. 3.
    Dexter, T. M. (1979) Clinical Haematology 8, 453–468 (Lajtha, L., ed.), W. B. Saunders, Philadelphia, PA.Google Scholar
  4. 4.
    Wolf, N. S. and Trentin, J. J. (1968) J. Exp. Med. 127, 205–214.PubMedGoogle Scholar
  5. 5.
    Curry, J. L. and Trentin, J. J. (1967) Dev. Biol. 15, 395–413.PubMedGoogle Scholar
  6. 6.
    Curry, J. L., Trentin, J. J., and Wolf, N. (1967) J. Exp. Med. 125, 703–719.PubMedGoogle Scholar
  7. 7.
    Quesenberry, P., Halperin, J., Ryan, M., and Stohlman, Jr., F. (1975) Blood 45, 789–800.PubMedGoogle Scholar
  8. 8.
    Quesenberry, P. J., Levin, J., Zuckerman, K., Rencricca, N., Sullivan, R., and Tyler, W. (1979) Br. J. Haematol. 41, 253–269.PubMedGoogle Scholar
  9. 9.
    McCulloch, E. A., Siminovitch, L., Till, J. E., Russell, E. S., and Bernstein, S. E. (1965) Blood 26, 399–410.PubMedGoogle Scholar
  10. 10.
    Bernstein, S. E. (1970) Am. J. Surg. 119, 448–151PubMedGoogle Scholar
  11. 11.
    Bessis, M., Miye, C., and Prenant, M. (1978) Blood Cells 4, 155–174.PubMedGoogle Scholar
  12. 12.
    Lichtman, M. A. (1981) Exp. Hematol. 9, 391–10.PubMedGoogle Scholar
  13. 13.
    Weiss, L. (1976) Anat. Rec. 186, 161–184.PubMedGoogle Scholar
  14. 14.
    Weiss, L. and Che, L.-T. (1975) Blood Cells 1, 617–638.Google Scholar
  15. 15.
    Weiss, L. (1970) Blood 36, 189–207.PubMedGoogle Scholar
  16. 16.
    Chamberlain, J. K., Leblond, P. R, and Weed, R. I. (1975) Blood Cells 1, 655–674.Google Scholar
  17. 17.
    Ito, J. (1965) Bull. Tokyo Med. Dent. Univ. 12, 1–28.PubMedGoogle Scholar
  18. 18.
    Zamboni, L., and Pease, D. C. (1961) J. Ultrastruct. Res. 5, 65–85.PubMedGoogle Scholar
  19. 19.
    Westen, H. and Bainton, D. F. (1979) J. Exp. Med. 150, 919–937.PubMedGoogle Scholar
  20. 20.
    Whitlock, C. A. and Witte, O. N. (1982) Proc. Natl. Acad. Sci. 79, 3608–3612.PubMedGoogle Scholar
  21. 21.
    Whitlock, C. A., Robertson, D., and Witte, O. N. (1984) J. Immunol. Method 67, 353–369.Google Scholar
  22. 22.
    Sakakeeny, M. A. and Greenberger, J. S. (1982) J. Natl. Can. Inst. 68, 305–317.Google Scholar
  23. 23.
    Quesenberry, P. J., Coppola, M. A., Gualtieri, R. J., Wade, P. J., Song, Z. X., Doukas, M. A., Shideler, C. E., Baker, D. G., and McGrath, H. E. (1984) Blood 63, 121–127.PubMedGoogle Scholar
  24. 24.
    Eliason, J. F. (1984) Exp. Hematol. 12, 559–567.PubMedGoogle Scholar
  25. 25.
    Dexter, T. M. (1982) J. Cell. Physiol. 1, 87–94.Google Scholar
  26. 26.
    Reimann, J. and Burger, H. (1979) Exp. Hematol. 7, 52–58.PubMedGoogle Scholar
  27. 27.
    Mauch, P., Greenberger, J. S., Hannon, E. C., and Hellman, S. (1980) Proc. Natl. Acad. Sci. 77, 2927–2930.PubMedGoogle Scholar
  28. 28.
    Dexter, T. M. and Moore, M. A. S. (1977) Nature 269, 412–414.PubMedGoogle Scholar
  29. 29.
    Greenberger, J. S. (1978) Nature 275, 752–754.PubMedGoogle Scholar
  30. 30.
    Levitt, L. J. and Quesenberry, P. J. (1980) N. Eng. J. Med. 302, 713–719.Google Scholar
  31. 31.
    McGrath, E., Liang, C., Alberico, T., and Quesenberry, P. (1987) Blood 70, 1136–1142.PubMedGoogle Scholar
  32. 32.
    Doukas, M., Niskanen, E., and Quesenberry, P. J. (1986) Exp. Hematol. 14, 215–221.PubMedGoogle Scholar
  33. 33.
    Wade, P. and Quesenberry, P. J. (1983) J. Cell. Biochem. (Suppl. 7B) (Fox, C.F., ed.), Liss, New York, NY, p. 30.Google Scholar
  34. 34.
    Hodgson, G. S. and Bradley, T. R. (1979) Cancer Treat. Rep. 63, 1761–1769.PubMedGoogle Scholar
  35. 35.
    Alberico, T., Ihle, J., and Quesenberry, P. (1987) Blood 69, 1120–1127.PubMedGoogle Scholar
  36. 36.
    Dorshkind, K. and Phillips, R. A. (1982) J. Immunol. 129, 2444–2450.PubMedGoogle Scholar
  37. 37.
    Schrader, J. W. and Schrader, S. (1978) J. Exp. Med. 148, 823–828.PubMedGoogle Scholar
  38. 38.
    Tavassoli, M. and Takahashi, K. (1982) Am. J. Anat. 164, 91–111.PubMedGoogle Scholar
  39. 39.
    Song, Z. X. and Quesenberry, P. J. (1984) Exp. Hematol. 12, 523–533.PubMedGoogle Scholar
  40. 40.
    Weiss, L. and Fawcett, D. W. (1953) J. Histochem. Cytochem. 1, 47–65.PubMedGoogle Scholar
  41. 41.
    Sutton, J. S. and Weiss, L. (1966) J. Cell Biol. 28, 303–332.PubMedGoogle Scholar
  42. 42.
    Gualtieri, R. J., Shadduck, R. K., and Quesenberry, P. J. (1984) Blood 64, 516–525.PubMedGoogle Scholar
  43. 43.
    Dexter, T. M., Spooncer, E., Simmons, P., and Allen, T. D. (1984) Long-Term Marrow Cultures (Wright, D. C. and Greenberger, J. S., eds.), Liss, New York, pp. 57–96.Google Scholar
  44. 44.
    Bentley, S. A. and Foidart, J. M. (1980) Blood 56, 1006–1012.PubMedGoogle Scholar
  45. 45.
    Bentley, S. A. and Tralka, T. S. (1982) Scand. J. Haematol. 28, 381–388.PubMedGoogle Scholar
  46. 46.
    Zuckerman, K. S. and Wicha, M. S. (1983) Blood 61, 540–547.PubMedGoogle Scholar
  47. 47.
    Waterhouse, E. J., Quesenberry, P. J., and Balian, G. (1986) J. Cell. Physiol. 127, 397–402.PubMedGoogle Scholar
  48. 48.
    Benya, P. D., Padilla, S. R., and Nimni, M. E. (1978) Cell 15, 1313–1321.PubMedGoogle Scholar
  49. 49.
    Allen, T. D. and Dexter, T. M. (1976) Differentiation 6, 191–194.PubMedGoogle Scholar
  50. 50.
    Gordon, M. Y., Goldman, J. M., and Gordon-Smith, E. C. (1983) Int. J. Cell Cloning 1, 429–139.PubMedGoogle Scholar
  51. 51.
    Touw, I. and Lowenberg, B. (1983) Blood 61, 770–774.PubMedGoogle Scholar
  52. 52.
    Simmons, P. J., Allen, T. D., Dexter, T. M., Hirsh, S., and Gordon, S. (1983) Exp. Hematol. 14, 144.Google Scholar
  53. 53.
    Tavassoli, M. and Shaklai, M. (1979) Br. J. Haematol. 43, 235–241.PubMedGoogle Scholar
  54. 54.
    Campbell, F. R. (1980) Anat. Rec. 196, 101–117.PubMedGoogle Scholar
  55. 55.
    Tavassoli, M. (1982) Exp. Hematol. 10, 435–443.PubMedGoogle Scholar
  56. 56.
    Crouse, D. A., Mann, S. L., Anderson, R. W., and Grazulewicz, S. (1980) Exp. Hematol. 8, 94.Google Scholar
  57. 57.
    Heard, J. M., Fichelson, S., and Varet, B. (1982) Blood 59, 761–767.PubMedGoogle Scholar
  58. 58.
    Williams, N., Jackson, H., Sheridan, A. P. C., Murphy, M. J., Elste, A., and Moore, M. A. S. (1978) Blood 51, 245–255.PubMedGoogle Scholar
  59. 59.
    Dexter, T. M. and Shadduck, R. K. (1980) J. Cell. Physiol. 102, 279, 280.Google Scholar
  60. 60.
    Ihle, J. N., Keller, J., Henderson, L., Klein, F., and Palaszynski, E. (1982) J. Immunol. 129, 2431–2436.PubMedGoogle Scholar
  61. 61.
    Greenberger, J. S., Sakakeeny, M. A., Krensky, A., Burakoff, S., Reid, D., Novak, T., and Boggs, S. (1984) Long Term Bone Marrow Culture, (Wright, D. G. and Greenberger, J. S., eds.), Liss, New York, pp. 255–269.Google Scholar
  62. 62.
    Ihle, J. N., Keller, J., Greenberger, J. S., Henderson, L., Yetter, R. A., and Morse, H. C., III (1982) J. Immunol. 129, 1377.PubMedGoogle Scholar
  63. 63.
    McGrath, H. E., Quesenberry, P. J., and Alberico, T., unpublished data.Google Scholar
  64. 64.
    Toksoz, D., Dexter, T. M., Lord, B. I., Wright, E. C., and Lajtha, L. G. (1980) Blood 55, 931–936.PubMedGoogle Scholar
  65. 65.
    Eastment, C. E. and Ruscetti, F. W. (1984) Long Term Bone Marrow Culture (Wright, D. G. and Greenberger, J. S., eds.) Liss, New York, pp. 97–118.Google Scholar
  66. 66.
    Shah, G., Dexter, T. M., and Lanotte, M. (1983) Br. J. Haematol. 54, 362–372.Google Scholar
  67. 67.
    Lomedico, P. T., Gubler, U., Hellman, C. P., Dukovich, M., Giri, J. G., Pan, Y. E., Collier, K., Semionow, R., Chua, A. O., and Mizel, S. B. (1984) Nature 312, 45–462.Google Scholar
  68. 68.
    Zipori, D., Reichman, N., Arravi, L., Shtalrid, M., Berrebi, A., and Resnitzky, P. (1985) Exp. Hematol. 13, 603–609.PubMedGoogle Scholar
  69. 69.
    Lauer, J., Ebell, W., and Castro-Malaspina, H. (1986) Blood 67, 1090–1097.Google Scholar
  70. 70.
    Castro-Malaspina, H., Gay, R. E., Jhanwar, S. C., Hamilton, J. A., Chiarieri, D. R., Meyers, P. A., Gay, S., and Moore, M. A. S. (1982) Blood 59, 1046–1054.PubMedGoogle Scholar
  71. 71.
    Castro-Malaspina, H., Gay, R. E., Resnick, G., Kapoor, N., Meyers, P., Chiareri, D., McKenzie, S., Broxmeyer, H. E., and Moore, M. A. S. (1980) Blood 56, 289–301.PubMedGoogle Scholar
  72. 72.
    Piersma, A. H., Brockbank, K. G. M., Ploemacher, R. E., Uliet, E., Brakel Van Peer, K. M., and Visser, P. J. (1985) Exp. Hematol. 13, 237–243.PubMedGoogle Scholar
  73. 73.
    Eastment, C. E., Denholm, E., Katznelson, I., Arnold, E., T’so, P. (1982) Blood 60, 130–135.PubMedGoogle Scholar
  74. 74.
    Moore, M. A. S., Sheridan, A. P. C., Allen, T. D., and Dexter, T. M. (1979) Blood 54, 775–793.PubMedGoogle Scholar
  75. 75.
    Gartner, S. and Kaplan, H. (1980) Proc. Natl Acad. Sci. 77, 4756–4759.PubMedGoogle Scholar
  76. 76.
    Dexter, T. M., Testa, N. G., Allen, T. D., Rutherford, T., and Scolnick, E. (1981) Blood 58, 699–707.PubMedGoogle Scholar
  77. 77.
    Eastment, C. E. and Ruscetti, F. W. (1982) Blood 60, 999–1006.PubMedGoogle Scholar
  78. 78.
    Coulombel, L., Eaves, A. C., and Eaves, C. J. (1983) Blood 62, 291–297.PubMedGoogle Scholar
  79. 79.
    Greenberg, H. M., Newburger, P. E., Parker, L. M., Novak, T., and Greenberger, J. S. (1981) Blood 58, 724–732.PubMedGoogle Scholar
  80. 80.
    Singer, J. W. (1984) Long Term Bone Marrow Culture, (Wright, D. G. and Greenberger, J. S., eds.), Liss, New York, pp. 235–242.Google Scholar
  81. 81.
    Golde, D. W., Hocking, W. G., Quan, S. G., Sparkes, R. S., and Gale, R. P. (1980) Br. J. Haematol. 53, 183–187.Google Scholar
  82. 82.
    Wilson, F. D., Greenberg, B. R., Konrad, P. N., Klein, A. K., and Walling, P. A. (1978) Transplantation 25, 87, 88.PubMedGoogle Scholar
  83. 83.
    Keating, A., Singer, J. W., Killen, P. D., Striker, G. E., Salo, A. C., Sanders, J., Thomas, E. D., Thorning, D., and Fialkow, P. J. (1982) Nature 298, 280–283.PubMedGoogle Scholar
  84. 84.
    Keating, A., Powell, J., Takahashi, M., and Singer, J. W. Blood (in press).Google Scholar
  85. 85.
    Gordon, M. Y. (1982) Stem Cells 1, 80.Google Scholar
  86. 86.
    Brockbank, K. G. M. and Van Peer, C. M. J. (1983) Acta Hematol. 69, 309.Google Scholar
  87. 87.
    Shibata, T. and Inoue, S. (1986) Exp.Hematol 14, 234-240.Google Scholar
  88. 88.
    Touw, I. and Lowenberg, B. (1984) Blood 64, 656.Google Scholar
  89. 89.
    Singer, J. W., Keating, A., Cattner, J., Gown, A. M., Jacobson, R., Killen, P. D., Moohr, J. W., Najfeld, V., Powell, J., Sanders, J., Striker, G. E., and Fialkow, P. J. (1984) Leuk. Res. 8, 535.PubMedGoogle Scholar
  90. 90.
    Eastment, C. E., Ruscetti, F. W., Denholm, E., Katznelson, I., Arnold, E., and T’so, P. (1982) Blood 60, 495–502.PubMedGoogle Scholar
  91. 91.
    Aspinall, R. and Owen, J. J. T. (1983) Immunology 48, 9–15.PubMedGoogle Scholar
  92. 92.
    Jones-Villeneuve, E. and Phillips, R. A. (1980) Exp. Hematol. 8, 65–76.PubMedGoogle Scholar
  93. 93.
    Schrader, J. W., Goldschneider, I., Bollum, F. J., and Schrader, S. (1979) J. Immunol. 122, 2337–2339.PubMedGoogle Scholar
  94. 94.
    Schrader, J. W., Schrader, S., Clark-Lewis, I., and Crapper, R. (1984) Long Term Bone Marrow Culture, (Wright, D. G. and Greenberger, J. S., eds.), Liss, New York, pp. 293–307.Google Scholar
  95. 95.
    Hocking, W. G. and Golde, D. W. (1980) Blood 56, 118–124.PubMedGoogle Scholar
  96. 96.
    Dorshkind, K. (1983) J. Immunol. 131, 2240–2245.PubMedGoogle Scholar
  97. 97.
    Kincade, P. W., Witte, P. L., and Landreth, K. S. (1986) Current Topics in Microbiology and Immunology (Gisler, R. and Paige, C., eds.), Springer (in press).Google Scholar
  98. 98.
    Kincade, P. W., Lee, G., Paige, C. F., and Scheid, M. P. (1981) J. Immunol. 127, 255–260.PubMedGoogle Scholar
  99. 99.
    Gisler, R. H., Paige, J., and Hollander, G. (1984) Immunobiol. 1114 (in press).Google Scholar
  100. 100.
    Phillips, R. A., Bosma, M., and Dorshkind, K. (1984) Long Term Bone Marrow Culture, (Wright, D.G. and Greenberger, J. S., eds.), Liss, New York, pp. 309–321.Google Scholar
  101. 101.
    Kurland, J. I., Ziegler, S. F., and Witte, O. N. (1984) Proc. Natl Acad. Sci. 81, 7554–7558.PubMedGoogle Scholar
  102. 102.
    Noelle, R., Krammer, P. H., O’Hara, J., Uhr, J. W., and Vitetta, E. S. (1984) Proc. Natl Acad. Sci. 81, 6149–6153.PubMedGoogle Scholar
  103. 103.
    Swain, S. L. and Dutton, R. W. (1982) J. Exp. Med. 156, 1821–1834.PubMedGoogle Scholar
  104. 104.
    Landreth, K. S., Engelhard, D., Beare, M. H., Kincade, P. W., and Good, R. A. (1984) Fed.Proc. 43, 1485 (abstract).Google Scholar
  105. 105.
    Landreth, K. S., Engelhard, D., Beare, M. H., Kincade, P. W., Kapoor, N., and Good, R. A. (1985) J. Immunol. 1134, 2305–2309.Google Scholar
  106. 106.
    Engelhard, D., Landreth, K. S., Kapoor, N., Kincade, P. W., DeBault, L. E., Theodore, A., and Good, R. A. (1983) Proc. Natl. Acad. Sci. 80, 5734–5738.PubMedGoogle Scholar
  107. 107.
    Landreth, K. S., Kincade, P. W., Lee, G., and Medlock, E. S. (1983) J. Immunol. 131, 572–580.PubMedGoogle Scholar
  108. 108.
    Landreth, K. S., Kincade, P. W., Lee, G., and Harrison, D. (1984) J. Immunol. 132, 2724–2729.PubMedGoogle Scholar
  109. 109.
    Medlock, E. S., Landreth, K. S., and Kincade, P. W. (1984) Dev. Comp. Immunol. 8, 887.PubMedGoogle Scholar
  110. 110.
    Landreth, K. S. and Kincade, P. W. (1984) Dev. Comp. Immunol. 8, 773, ai]111_Quesenberry, P. J., and Landreth, K. S., unpublished data.PubMedGoogle Scholar
  111. 112.
    Bradley, T. R. and Hodgson, G. S. (1979) Blood 54, 1446–1450.PubMedGoogle Scholar
  112. 113.
    Bradley, T. R., Kriegler, A. B., McNiece, I. K., and Hodgson, G. S. (1982) Exp. Hematol. 10, 10.Google Scholar
  113. 114.
    Quesenberry, P. J., Song, Z. X., Gualtieri, R. J., Wade, Jr., P. M., Alberico, T. A., Stewart, F. M., Doukas, M. A., Levitt, L., McGrath, H. E., Rexrode, L. A., and Innes, D. J. (1984) Long Term Bone Marrow Culture, (Wright, D. G. and Greenberger, J. S., eds.), Liss, New York, pp. 171–193.Google Scholar
  114. 115.
    Quesenberry, P. J., Song, Z., McGrath, E., Shadduck, R., Waheed, A., Baber, G., Kleeman, E., and Kaiser, D. (1987) Blood 69, 827–835.PubMedGoogle Scholar
  115. 116.
    Quesenberry, P. J. and Isakson, P. C., unpublished data.Google Scholar
  116. 117.
    Johnson, A. and Dorshkind, K. (1986) Blood (in press).Google Scholar
  117. 118.
    Quesenberry, P. J., Ihle, J. N., and McGrath, H. E. (1985) Blood 65, 214–217.PubMedGoogle Scholar

Copyright information

© The Humana Press Inc. 1989

Authors and Affiliations

  • Peter J. Quesenberry

There are no affiliations available

Personalised recommendations