Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1990 Jan 1;265(1):243–249. doi: 10.1042/bj2650243

Synergistic activation of 2-deoxy-D-glucose uptake in rat and murine peritoneal macrophages by human macrophage colony-stimulating factor-stimulated coupling between transport and hexokinase activity and phorbol-dependent stimulation of pentose phosphate-shunt activity.

R J Rist 1, G E Jones 1, R J Naftalin 1
PMCID: PMC1136636  PMID: 2405838

Abstract

1. Transport and accumulation of 2-deoxy-D-glucose (2dGlc) in rat and murine peritoneal macrophages were investigated by using C-1-3H-labelled and C-2,6-3H-labelled 2dGlc. 2. There was active accumulation of both C-1- and C-2,6-labelled 2dGlc by quiescent rat and murine macrophages via a phloretin-inhibitable transport system. 3. The rate of uptake and accumulation of 2dGlc (C-1 label) was increased by exposure to human macrophage colony-stimulating factor (mCSF-1) (1000 units/ml) in both murine and rat macrophages. This indicates that mCSF-1 enhances coupling between hexokinase activity and glucose transport at the endofacial surface of the transporter. 4. Phorbol 12-myristate 13-acetate ('phorbol') at 40 nM stimulated 2dGlc in rat macrophages entirely by increasing the C-2,6 label uptake. This indicates that phorbol stimulates 2dGlc uptake mainly by increasing the activity of the pentose phosphate pathway. 5. Simultaneous exposure to phorbol and mCSF-1 stimulates 2dGlc uptake to a greater extent than found with either phorbol or mCSF-1 alone. This result is explained by a simultaneous enhancement of pentose phosphate-pathway activity and of hexokinase activity acting at the endofacial surface of the cell membrane. The dual activation of these serial processes coupled to the loss of the reaction products of the pentose phosphate-shunt pathway from the cells in the form of reactive oxygen intermediates, protons and CO2 could explain the synergistic action of phorbol and mCSF-1 in activation of sugar transport in macrophages.

Full text

PDF
243

Selected References

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

  1. Arthur M. J., Kowalski-Saunders P., Wright R. Corynebacterium parvum-elicited hepatic macrophages demonstrate enhanced respiratory burst activity compared with resident Kupffer cells in the rat. Gastroenterology. 1986 Jul;91(1):174–181. doi: 10.1016/0016-5085(86)90455-5. [DOI] [PubMed] [Google Scholar]
  2. Arthur M. J., Kowalski-Saunders P., Wright R. Effect of endotoxin on release of reactive oxygen intermediates by rat hepatic macrophages. Gastroenterology. 1988 Dec;95(6):1588–1594. doi: 10.1016/s0016-5085(88)80082-9. [DOI] [PubMed] [Google Scholar]
  3. Babior B. M., Peters W. A. The O2--producing enzyme of human neutrophils. Further properties. J Biol Chem. 1981 Mar 10;256(5):2321–2323. [PubMed] [Google Scholar]
  4. Badwey J. A., Karnovsky M. L. Active oxygen species and the functions of phagocytic leukocytes. Annu Rev Biochem. 1980;49:695–726. doi: 10.1146/annurev.bi.49.070180.003403. [DOI] [PubMed] [Google Scholar]
  5. Boocock C. A., Jones G. E., Stanley E. R., Pollard J. W. Colony-stimulating factor-1 induces rapid behavioural responses in the mouse macrophage cell line, BAC1.2F5. J Cell Sci. 1989 Jul;93(Pt 3):447–456. doi: 10.1242/jcs.93.3.447. [DOI] [PubMed] [Google Scholar]
  6. Donahue R. E., Seehra J., Metzger M., Lefebvre D., Rock B., Carbone S., Nathan D. G., Garnick M., Sehgal P. K., Laston D. Human IL-3 and GM-CSF act synergistically in stimulating hematopoiesis in primates. Science. 1988 Sep 30;241(4874):1820–1823. doi: 10.1126/science.3051378. [DOI] [PubMed] [Google Scholar]
  7. Faik P., Morgan M., Naftalin R. J., Rist R. J. Transport and accumulation of 2-deoxy-D-glucose in wild-type and hexokinase-deficient cultured Chinese-hamster ovary (CHO) cells. Biochem J. 1989 May 15;260(1):153–155. doi: 10.1042/bj2600153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gabig T. G. The NADPH-dependent O-.2-generating oxidase from human neutrophils. J Biol Chem. 1983 May 25;258(10):6352–6356. [PubMed] [Google Scholar]
  9. Hamilton J. A., Vairo G., Lingelbach S. R. Activation and proliferation signals in murine macrophages: stimulation of glucose uptake by hemopoietic growth factors and other agents. J Cell Physiol. 1988 Mar;134(3):405–412. doi: 10.1002/jcp.1041340311. [DOI] [PubMed] [Google Scholar]
  10. Hamilton J. A., Vairo G., Lingelbach S. R. CSF-1 stimulates glucose uptake in murine bone marrow-derived macrophages. Biochem Biophys Res Commun. 1986 Jul 16;138(1):445–454. doi: 10.1016/0006-291x(86)90301-3. [DOI] [PubMed] [Google Scholar]
  11. Jin C. H., Segawa A., Miyaura C., Tanaka H., Abe E., Suda T. Calcium is essential in the fusion of mouse alveolar macrophages induced by 1 alpha,25-dihydroxyvitamin D3. J Cell Physiol. 1988 Oct;137(1):110–116. doi: 10.1002/jcp.1041370113. [DOI] [PubMed] [Google Scholar]
  12. Miyaura C., Segawa A., Nagasawa H., Abe E., Suda T. Effects of retinoic acid on the activation and fusion of mouse alveolar macrophages induced by 1 alpha,25-dihydroxyvitamin D3. J Bone Miner Res. 1986 Aug;1(4):359–368. doi: 10.1002/jbmr.5650010409. [DOI] [PubMed] [Google Scholar]
  13. Naftalin R. J., Rist R. J. Effects of phorbol, dexamethasone and starvation on 3-O-methyl-D-glucose transport by rat thymocytes. Modulation of transport by altered trans effects. Biochem J. 1990 Jan 1;265(1):251–259. doi: 10.1042/bj2650251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Naftalin R. J., Rist R. J. Evidence that activation of 2-deoxy-D-glucose transport in rat thymocyte suspensions results from enhanced coupling between transport and hexokinase activity. Biochem J. 1989 May 15;260(1):143–152. doi: 10.1042/bj2600143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Naftalin R. J., Smith P. M. A model for accelerated uptake and accumulation of sugars arising from phosphorylation at the inner surface of the cell membrane. Biochim Biophys Acta. 1987 Feb 12;897(1):93–111. doi: 10.1016/0005-2736(87)90318-x. [DOI] [PubMed] [Google Scholar]
  16. Newsholme P., Curi R., Gordon S., Newsholme E. A. Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages. Biochem J. 1986 Oct 1;239(1):121–125. doi: 10.1042/bj2390121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Newsholme P., Gordon S., Newsholme E. A. Rates of utilization and fates of glucose, glutamine, pyruvate, fatty acids and ketone bodies by mouse macrophages. Biochem J. 1987 Mar 15;242(3):631–636. doi: 10.1042/bj2420631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rest R. F., Farrell C. F., Naids F. L. Mannose inhibits the human neutrophil oxidative burst. J Leukoc Biol. 1988 Feb;43(2):158–164. doi: 10.1002/jlb.43.2.158. [DOI] [PubMed] [Google Scholar]
  19. Towler D. A., Gordon J. I., Adams S. P., Glaser L. The biology and enzymology of eukaryotic protein acylation. Annu Rev Biochem. 1988;57:69–99. doi: 10.1146/annurev.bi.57.070188.000441. [DOI] [PubMed] [Google Scholar]
  20. Walker F., Nicola N. A., Metcalf D., Burgess A. W. Hierarchical down-modulation of hemopoietic growth factor receptors. Cell. 1985 Nov;43(1):269–276. doi: 10.1016/0092-8674(85)90032-7. [DOI] [PubMed] [Google Scholar]
  21. Whetton A. D., Heyworth C. M., Dexter T. M. Phorbol esters activate protein kinase C and glucose transport and can replace the requirement for growth factor in interleukin-3-dependent multipotent stem cells. J Cell Sci. 1986 Aug;84:93–104. doi: 10.1242/jcs.84.1.93. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES