Skip to main content
SpringerLink
Log in

Simulated microgravity impairs respiratory burst activity in human promyelocytic cells

  • Special-Nasa/Johnson Space Center Workshop
  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Summary

The concept of microgravity (free-fall) influencing cellular functions in nonadherent cells has not been a part of mainstream scientific thought. Utilizing rotating wall vessels (RWVs) to generate simulated microgravity conditions, we found that respiratory burst activity was significantly altered in nonadherent promyelocytic (HL-60) cells. Specifically, HL-60 cells in simulated microgravity for 6, 19, 42, 47, and 49 d had 3.8-fold fewer cells that were able to participate in respiratory burst activity than cells from 1×g cultures (P=0.0011, N=5). The quantity of respiratory burst products from the cells in simulated microgravity was also significantly reduced. The fold increase over controls in mean fluorescence intensities for oxidative products from cells in microgravity was 1.1±0.1 versus 1.8±0.3 for cells at 1 ×g (P=0.013, N=4). Furthermore, the kinetic response for phorbol ester-stimulated burst activity was affected by simulated microgravity. These results demonstrate that simulated microgravity alters an innate cellular function (burst activity). If respiratory burst activity is impaired by true microgravity, then recovery from infections during spaceflight could be delayed. Finally, RWVs provide an excellent model for investigating the mechanisms associated with microgravity-induced changes in nonadherent cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Babior, B. M. Oxygen-dependent microbial killing by phagocytes. N. Engl. J. Med. 298:659–668; 1978.

    Article  PubMed  CAS  Google Scholar 

  • Baker, T. L.; Goodwin, T. J. Three-dimensional culture of bovine chondrocytes in rotating-wall vessels. In Vitro Cell. Dev. Biol. 33A:358–365; 1997.

    Article  Google Scholar 

  • Bechler, B.; Cogoli, A.; Cogoli-Creuter, M., et al. Activation of microcarrierattached lymphocytes in microgravity. Biotech. Bioeng. 40:991–996; 1992.

    Article  CAS  Google Scholar 

  • Becker, J. L.; Prewett, T. L.; Spaulding, G. F., et al. Three-dimensional growth and differentiation of ovarian tumor cell line in high aspect rotating-wall vessel: morphologic and embryologic considerations. J. Cell. Biochem. 51:283–289; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Cao, D.; Boxer, L. A.; Petty, H. R. Deposition of reactive oxygen metabolites onto and within living tumor cells during neutrophil-mediated antibody-dependent cellular cytotoxicity. J. Cell Physiol. 156:428–436; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Chapes, S. K.; Morrison, D. R.; Guikema, J. A., et al. Cytokine secretion by immune cells in space. J. Leukoc. Biol. 52:104–110; 1992.

    PubMed  CAS  Google Scholar 

  • Cogoli, A. The effect of hypogravity and hypergravity on cells of the immune system. J. Leukoc. Biol. 54:259–268; 1993.

    PubMed  CAS  Google Scholar 

  • Cogoli, A.; Bechler, B.; Cogoli-Greuter, M., et al. Mitogenic signal transduction in T lymphocytes in microgravity. J. Leukoc. Biol. 53:569–575; 1993.

    PubMed  CAS  Google Scholar 

  • Cogoli, A.; Cogoli-Greuter, M. Activation and proliferation of lymphocytes and other mammalian cells in microgravity. Adv. Space Biol. Med. 6:33–79; 1997.

    PubMed  CAS  Google Scholar 

  • Cogoli, A.; Valluchi-Morf, M.; Mueller, M., et al. Effect of hypogravity on human lymphocyte activation. Aviat. Space Environ. Med. 51:29–34; 1980.

    PubMed  CAS  Google Scholar 

  • Cogoli, M. The fast rotating clinostat: a history of its use in gravitational biology and a comparison of ground-based and flight experiment results. Am. Soc. Gravit. Space Biol. Bull. 5(2):59–67; 1992.

    CAS  Google Scholar 

  • Collins, S. J. The HL-60 promyelocytic leukemia cell line: proliferation, differentiation, and cellular oncogene expression. Blood 70(5):1233–1244; 1987.

    PubMed  CAS  Google Scholar 

  • Cooper, D.; Pellis, N. R. Suppressed PHA activation of T lymphocytes in simulated microgravity is restored by direct activation of protein kinase C. J. Leukoc. Biol. 63:550–562; 1998.

    PubMed  CAS  Google Scholar 

  • Duray, P. H.; Hatfill, S. J.; Pellis, N. R. Tissue culture in microgravity. Sci. Med. May/June:46–55; 1997.

    Google Scholar 

  • Emmendörffer, A.; Hecht, M.; Lohmann-Matthes, M.-L., et al. A fast and easy method to determine the production of reactive oxygen intermediates by human and murine phagocytes using dihydrorhodamine 123. J. Immunol. Methods 131:269–275; 1990.

    Article  PubMed  Google Scholar 

  • Fleming, S. D.; Edelman, L. S.; Chapes, S. K. Effects of corticosterone and microgravity on inflammatory cell production of superoxide. J. Leukoc. Biol. 50:69–76; 1991.

    PubMed  CAS  Google Scholar 

  • Freed, L. E.; Langer, R.; Martin, I., et al. Tissue engineering of cartilage in space. Proc. Natl. Acad. Sci. USA 94:13,885–13,890; 1997.

    Article  CAS  Google Scholar 

  • Glasser, L.; Fiederlein, R. L. The effect of various cell separation procedures on assays of neutrophil function. Am. J. Clin. Pathol. 93:662–669; 1990.

    PubMed  CAS  Google Scholar 

  • Gmünder, F. K.; Cogoli, A. Effect of spaceflight on lymphocyte function and immunity, chapter 35. In: Fregly, M. J.; Blatteis, C. M., ed. Handbook of physiology. New York: Oxford University Press; 1996:799–813.

    Google Scholar 

  • Goodwin, T. J.; Prewett, T. L.; Spaulding, G. F., et al. Three-dimensional culture of a cell line from mixed mullerian tumor of the ovary: expression ofin vivo characteristics. In Vitro Cell. Dev. Biol. 33A:366–374; 1997.

    Article  Google Scholar 

  • Goodwin, T. J.; Prewett, T. L.; Wolf, D. A., et al. Reduced shear stress: a major component in the ability of mammalian tissues to form three-dimensional assemblies in simulated microgravity. J. Cell. Biochem. 51:301–311; 1993a.

    Article  PubMed  CAS  Google Scholar 

  • Goodwin, T. J.; Schroeder, W. F.; Wolf, D. A., et al. Rotating-wall vessel coculture of small intestine as a prelude to tissue modeling: aspects of simulated microgravity. Proc. Soc. Exp. Biol. Med. 202:181–192; 1993b.

    PubMed  CAS  Google Scholar 

  • Hammond, T. G.; Lewis, F. C.; Goodwin, T. J., et al. Gene expression in space. Nat. Med. 5:359; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Hashemi, B. B.; Penkala, J. E.; Vens, C., et al. T cell activation responses are differentially regulated during clinorotation and in spaceflight. FASEB J. 13:2071–2082; 1999.

    PubMed  CAS  Google Scholar 

  • Hatton, J. P.; Gaubert, F.; Lewis, M. L., et al. The kinetics of translocation and cellular quantity of protein kinase C in human leukocytes are modified during spaceflight. FASEB J. 13(Suppl.):S23-S33; 1999.

    PubMed  CAS  Google Scholar 

  • Henderson, L. M.; Chappell, J. B. Dihydrorhodamine 123: a fluorescent probe for superoxide generation?. Eur. J. Biochem. 217:973–980; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Jessup, J. M.; Goodwin, T. J.; Spaulding, G. Prospects for use of microgravity-based bioreactors to study three-dimensional host-tumor interactions in human neoplasia. J. Cell. Biochem. 51:290–300; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Khaoustov, V. I.; Darlington, G. J.; Soriano, H. E., et al. Induction of three-dimensional assembly of human liver cells by simulated microgravity. In Vitro Cell. Dev. Biol. 35A:501–509; 1999.

    Article  Google Scholar 

  • Konstantinova, I. V.; Sonnenfeld, G.; Lesnyak, A. T., et al. Cellular immunity and lymphokine production during spaceflights. Physiologist 34:S52-S56; 1991.

    PubMed  CAS  Google Scholar 

  • Kuijpers, T. W.; Tool, A. T. J.; van der Schoot, C. E., et al. Membrane surface antigen expression on neutrophils: a reappraisal of the use of surface markers for neutrophil activation. Blood 78:1105–1111; 1991.

    PubMed  CAS  Google Scholar 

  • Levy, R.; Rotrosen, D.; Nagauker, O., et al. Induction of the respiratory burst in HL-60 cells—correlation of function and protein expression. J. Immunol. 145:2595–2601; 1990.

    PubMed  CAS  Google Scholar 

  • Licato, L. L.; Grimm, E. A. Multiple interleukin-2 signaling pathways differentially regulated by microgravity. Immunopharmacology 44:273–279; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Margolis, L. B.; Fitzgerald, W.; Glushakova, S., et al. Lymphocyte trafficking and HIV infection of human lymphoid tissue in a rotating wall vessel bioreactor. AIDS Res. Hum. Retroviruses 13:1411–1420; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Meehan, R. T.; Neale, L. S.; Kraus, E. T., et al. Alteration in human mononuclear leucocytes following space flight. Immunology 76:491–497; 1992.

    PubMed  CAS  Google Scholar 

  • Pellis, N. R.; Goodwin, T. J.; Risin, D., et al. Changes in gravity inhibit lymphocyte locomotion through type I collagen. In Vitro Cell. Dev. Biol. 33A:398–405; 1997.

    Article  Google Scholar 

  • Pippia, P.; Sciola, L.; Cogoli-Greuter, M., et al. Activation signals of T lymphocytes in microgravity. J. Biotechnol. 47:215–222; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Prewett, T. L.; Goodwin, T. J.; Spaulding, G. F. Three-dimensional modeling of T-24 human bladder carcinoma cell line: a new simulated microgravity culture vessel. J. Tissue Cult. Methods 15:29–36; 1993.

    Article  Google Scholar 

  • Richardson, M. P.; Ayliffe, M. J.; Helbert, M., et al. A simple flow cytometry assay using dihydrorhodamine for the measurement of the neutrophil respiratory burst in whole blood: comparison with the quantitative nitrobluetetrazolium test. J. Immunol. Methods 219:187–193; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Rijken, P. J.; deGroot, R. P.; Kruijer, W., et al. Altered gravity conditions affect early EGF-induced signal transduction in human epidermal A431 cells. ASGSB Bull. 5(2):77–82; 1992.

    PubMed  CAS  Google Scholar 

  • Rothe, G.; Emmendörffer, A.; Oser, A., et al. Flow cytometric measurement of the respiratory burst activity of phagocytes using dihydrorhodamine 123. J. Immunol. Methods 138:133–135; 1991.

    Article  PubMed  CAS  Google Scholar 

  • Salgar, S. K.; Paape, M. J.; Alston-Mills, B., et al. Flow cytometric study of oxidative burst activity in bovine neutrophils. Am. J. Veterinary Res. 52:1201–1207; 1991.

    CAS  Google Scholar 

  • Schwarz, R. P.; Goodwin, T. J.; Wolf, D. A. Cell culture for three-dimensional modeling in rotating-wall vessels: an application of simulated microgravity. J. Tissue Cult. Methods 14:51–58; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Schwarz, R. P.; Wolf, D. A. Rotating bio-reactor cell culture apparatus. Patent No. 4,988,623; 1991.

  • Schwarz, R. P.; Wolf, D. A.; Trinh, T. T. Horizontally rotated cell culture system with a coaxial tubular oxygenator. Patent No. 5,026,650; 1991.

  • Sonnenfeld, G.; Immune responses in space flight. Int. J. Sports Med. 19:S195-S204; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Stowe, R. P.; Sams, C. F.; Mehta, S. K., et al. Leukocyte subsets and neutrophil function after short-term spaceflight. J. Leukoc. Biol. 65:179–186; 1999.

    PubMed  CAS  Google Scholar 

  • Taylor, G. R. Overview of spaceflight immunology studies. J. Leukoc. Biol. 54:179–188; 1993.

    PubMed  CAS  Google Scholar 

  • Taylor, G. R.; Konstantinova, I.; Sonnenfeld, G., et al. Changes in the immune system during and after spaceflight. Adv. Space Biol. Med. 6:1–32; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Tipton, C. M.; Greenleaf, J. F.; Jackson, C. G. R. Neuroendocrine and immune system responses with spaceflights. Med. Sci. Sports Exerc. 28:988–998; 1996.

    PubMed  CAS  Google Scholar 

  • Unsworth, B. R.; Lelkes, P. I. Growing tissues in microgravity. Nat. Med. 4:901–907; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Walther, I.; Pippia, P.; Meloni, M. A., et al. Simulated microgravity inhibits the genetic expression of interleukin-2 and its receptor in mitogen-activated T lymphocytes. FEBS Lett. 436:115–118; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Zhau, H. E.; Goodwin, T. J.; Chang, S.-M., et al. Establishment of a three-dimensional human prostate organoid coculture under microgravity-simulated conditions: evaluation of androgen-induced growth and PSA expression. In Vitro Cell. Dev. Biol. 33A:375–380; 1997.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Virology, Immunology, and Medical Genetics, The Ohio State University, 43210, Columbus, Ohio

    John H. Hughes & James P. Long

  2. Children's Research Institute, 308 Wexner Institute, 700 Children's Drive, 43205, Columbus, Ohio

    John H. Hughes

Authors
  1. John H. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James P. Long
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John H. Hughes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hughes, J.H., Long, J.P. Simulated microgravity impairs respiratory burst activity in human promyelocytic cells. In Vitro Cell.Dev.Biol.-Animal 37, 209–215 (2001). https://doi.org/10.1007/BF02577531

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02577531

Key words

Search

Navigation