Abstract
We have tested the hypothesis that the rapid stimulation of Na+/H+ exchange by epidermal growth factor (EGF) is a requirement for induction of mitogenesis. BALB/c 3T3 cells exposed for 4 hr at 37 degrees C to both EGF at 1 ng/ml and either 0.2-1 mM amiloride (an inhibitor of Na+/H+ exchange) or 10 microM MK-685 (an amiloride analog and more potent inhibitor of Na+/H+ exchange) incorporated no less [methyl-3H]thymidine during a 1-hr pulse 20 hr later than did cells exposed for 4 hr to EGF alone. Control experiments utilizing low external pH (to dissociate EGF from its receptor) and anti-EGF antibodies indicated that the failure of amiloride to inhibit mitogenesis when copresent with EGF during the first 4 hr was not due to incomplete removal of EGF and complete removal of amiloride at t4. Cells incubated with 200 microM amiloride for 24 hr showed nearly complete inhibition of stimulation by EGF. In comparison, cells incubated with 10 microM MK-685 for 24 hr showed only a slight inhibition of stimulation by EGF. Incubations with amiloride or MK-685 for shorter periods of time indicated that only amiloride inhibited mitogenesis and that this inhibition happened between 4 (t4) and 10(t10) hr after EGF addition, during which time increases in RNA and protein synthesis (required for mitogenesis) occurred. Amiloride inhibited both RNA and protein syntheses in intact cells during this prereplicative period, while MK-685 was without effect. We conclude that (i) inhibition of EGF-induced mitogenesis by amiloride is due not to inhibition of EGF-stimulated Na+/H+ exchange but rather to inhibition of necessary events occurring during the hours immediately prior to the onset of DNA synthesis, these events probably being RNA and protein synthesis and (ii) in cell culture medium buffered with CO2/HCO3-, complete inhibition of EGF-stimulated Na+/H+ exchange does not inhibit EGF-induced mitogenesis and, thus, stimulation of Na+/H+ exchange is not necessary for induction of mitogenesis by EGF.
MeSH Terms
Amiloride/analogs & derivatives,pharmacology
Animals
Carrier Proteins/antagonists & inhibitors
Cell Line
Epidermal Growth Factor/pharmacology
Humans
Kinetics
Mice
Mice, Inbred BALB C
Mitosis/drug effects
Protein Biosynthesis
Protons
Pyrazines/pharmacology
RNA/biosynthesis
Sodium/metabolism
Sodium-Hydrogen Exchangers
Chemicals
Carrier Proteins
Protons
Pyrazines
Sodium-Hydrogen Exchangers
5-dimethylamiloride
Epidermal Growth Factor
RNA
Amiloride
Sodium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Besterman J M
Tyrey S J
Cragoe E J
Cuatrecasas P
References (26)
26 references, click to expand
-
The amiloride-sensitive Na+/H+ antiport in 3T3 fibroblasts.
J Biol Chem. 1983 May 25;258(10):6272-6
PMID: 6304031
-
Ionic responses and growth stimulation induced by nerve growth factor and epidermal growth factor in rat pheochromocytoma (PC12) cells.
J Cell Biol. 1983 Jul;97(1):92-8
PMID: 6306015
-
Two forms of murine epidermal growth factor: rapid separation by using reverse-phase HPLC.
Proc Natl Acad Sci U S A. 1982 Oct;79(19):5753-7
PMID: 6985267
-
Activation of Na+/H+ exchange by epidermal growth factor elevates intracellular pH in A431 cells.
J Biol Chem. 1983 Oct 25;258(20):12644-53
PMID: 6195155
-
Demonstration of a late amiloride-sensitive event as a necessary step in initiation of DNA synthesis by thrombin.
J Cell Physiol. 1983 Nov;117(2):272-81
PMID: 6630302
-
Blockade of the Na+/H+ antiport abolishes growth factor-induced DNA synthesis in fibroblasts. Structure-activity relationships in the amiloride series.
J Biol Chem. 1984 Apr 10;259(7):4313-9
PMID: 6323465
-
Phorbol esters rapidly stimulate amiloride-sensitive Na+/H+ exchange in a human leukemic cell line.
J Cell Biol. 1984 Jul;99(1 Pt 1):340-3
PMID: 6330130
-
Pyrazine diuretics. II. N-amidino-3-amino-5-substituted 6-halopyrazinecarboxamides.
J Med Chem. 1967 Jan;10(1):66-75
PMID: 6031705
-
Epidermal growth factor: effects of androgens and adrenergic agents.
Endocrinology. 1974 Sep;95(3):776-82
PMID: 4368688
-
Human epidermal growth factor and the proliferation of human fibroblasts.
J Cell Physiol. 1976 Jun;88(2):227-37
PMID: 944704
-
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem. 1976 May 7;72:248-54
PMID: 942051
-
Continuous protein synthesis is required to maintain the probability of entry into S phase.
Cell. 1977 Sep;12(1):311-7
PMID: 902318
-
Epidermal growth factor: biological activity requires persistent occupation of high-affinity cell surface receptors.
Proc Natl Acad Sci U S A. 1978 Dec;75(12):5788-91
PMID: 215996
-
Increased sodium ion influx is necessary to initiate rat hepatocyte proliferation.
Cell. 1979 Sep;18(1):153-63
PMID: 509519
-
Dansylcadaverine inhibits internalization of 125I-epidermal growth factor in BALB 3T3 cells.
J Biol Chem. 1980 Feb 25;255(4):1239-41
PMID: 6243633
-
Plasma concentrations of immunoreactive human epidermal growth factor (urogastrone) in man.
J Clin Endocrinol Metab. 1980 Mar;50(3):440-4
PMID: 6965677
-
Rapid ionic events and the initiation of growth in serum-stimulated neuroblastoma cells.
Cell. 1981 Mar;23(3):789-98
PMID: 6261956
-
Inhibition of mouse mastocytoma protein kinases by amiloride.
Biochem Biophys Res Commun. 1982 Feb 11;104(3):1054-9
PMID: 6280704
-
Epidermal growth factor induces electrically silent Na+ influx in human fibroblasts.
J Biol Chem. 1982 Jul 25;257(14):8502-6
PMID: 6979542
-
Growth factor activation of an amiloride-sensitive Na+/H+ exchange system in quiescent fibroblasts: coupling to ribosomal protein S6 phosphorylation.
Proc Natl Acad Sci U S A. 1982 Jul;79(13):3935-9
PMID: 6287453
-
Synthesis, turnover, and down-regulation of epidermal growth factor receptors in human A431 epidermoid carcinoma cells and skin fibroblasts.
J Biol Chem. 1982 Oct 10;257(19):11489-96
PMID: 6288686
-
Amiloride blocks cell-free protein synthesis at levels attained inside cultured rat hepatocytes.
Biochem Biophys Res Commun. 1982 Sep 30;108(2):738-45
PMID: 7150320
-
Na+/H+ antiport in Swiss 3T3 cells: mitogenic stimulation leads to cytoplasmic alkalinization.
Proc Natl Acad Sci U S A. 1982 Dec;79(24):7778-82
PMID: 6961450
-
Lys-bradykinin stimulates Na+ influx and DNA synthesis in cultured human fibroblasts.
Cell. 1983 Mar;32(3):979-85
PMID: 6339076
-
Persistence of the mitogenic response to platelet-derived growth factor (competence) does not reflect a long-term interaction between the growth factor and the target cell.
J Cell Biol. 1983 May;96(5):1497-502
PMID: 6841457
-
Amiloride directly inhibits the Na,K-ATPase activity of rabbit kidney proximal tubules.
Science. 1983 May 27;220(4600):957-8
PMID: 6302840