Temporal Relationship Between Inositol Polyphosphate Formation and Increases in Cytosolic Ca2+ in Quiescent 3T3 Cells Stimulated by Platelet-derived Growth Factor, Bombesin and Vasopressin

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1988 Sep 1

PMID 3181139

Citations 24

Authors

E Nanberg

E Rozengurt

Affiliations

Soon will be listed here.

Abstract

We determined the temporal relationship between the formation of inositol phosphates and increase in cytosolic [Ca2+] elicited by bombesin, vasopressin and platelet-derived growth factor (PDGF) in quiescent Swiss 3T3 cells. These responses were measured under identical conditions. Bombesin caused a rapid increase in inositol 1,4,5-trisphosphate which coincided with the increase in cytosolic [Ca2+]. This was followed by a slower but marked increase in inositol 1,3,4-trisphosphate and inositol-bisphosphate. Vasopressin elicited a similar sequence of events. In sharp contrast, highly purified porcine PDGF induced increases in cytosolic [Ca2+] and inositol 1,4,5-trisphosphate that were temporally uncoupled: detectable inositol polyphosphate formation occurred after Ca2+ mobilization from intracellular stores. The same temporal dissociation was observed when a recombinant v-sis product was used instead of porcine PDGF. However, PDGF was as effective as bombesin in stimulating the formation of inositol phosphates after 5-10 min of incubation. The data suggest that PDGF increases cytosolic [Ca2+] via a different signal transduction pathway from that utilized by bombesin and vasopressin. These findings have important implications for understanding the signal transduction pathway activated by PDGF.

Citing Articles

Phosphoinositides: tiny lipids with giant impact on cell regulation.

Balla T Physiol Rev. 2013; 93(3):1019-137.

PMID: 23899561 PMC: 3962547. DOI: 10.1152/physrev.00028.2012.

Histidine Residues at the Active Site of the Pasteurella multocida Toxin.

Pullinger G, Lax A Open Biochem J. 2008; 1:7-11.

PMID: 18949067 PMC: 2570546. DOI: 10.2174/1874091X00701010007.

Neuropeptide-induced androgen independence in prostate cancer cells: roles of nonreceptor tyrosine kinases Etk/Bmx, Src, and focal adhesion kinase.

Lee L, Guan J, Qiu Y, Kung H Mol Cell Biol. 2001; 21(24):8385-97.

PMID: 11713275 PMC: 100003. DOI: 10.1128/MCB.21.24.8385-8397.2001.

Leptin rapidly suppresses insulin release from insulinoma cells, rat and human islets and, in vivo, in mice.

Kulkarni R, Wang Z, Wang R, HURLEY J, Smith D, Ghatei M J Clin Invest. 1998; 100(11):2729-36.

PMID: 9389736 PMC: 508476. DOI: 10.1172/JCI119818.

Pasteurella multocida toxin is a mitogen for bone cells in primary culture.

Mullan P, Lax A Infect Immun. 1996; 64(3):959-65.

PMID: 8641807 PMC: 173863. DOI: 10.1128/iai.64.3.959-965.1996.

References

Lopez-Rivas A, Rozengurt E . Vasopressin rapidly stimulates Ca2+ efflux from intracellular pool in quiescent Swiss 3T3 cells. Am J Physiol. 1984; 247(3 Pt 1):C156-62. DOI: 10.1152/ajpcell.1984.247.3.C156. View

Moolenaar W, Tertoolen L, de Laat S . Growth factors immediately raise cytoplasmic free Ca2+ in human fibroblasts. J Biol Chem. 1984; 259(13):8066-9. View

Brown K, Blay J, Irvine R, Heslop J, Berridge M . Reduction of epidermal growth factor receptor affinity by heterologous ligands: evidence for a mechanism involving the breakdown of phosphoinositides and the activation of protein kinase C. Biochem Biophys Res Commun. 1984; 123(1):377-84. DOI: 10.1016/0006-291x(84)90424-8. View

Berridge M, Irvine R . Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984; 312(5992):315-21. DOI: 10.1038/312315a0. View

Hesketh T, Moore J, Morris J, Taylor M, Rogers J, Smith G . A common sequence of calcium and pH signals in the mitogenic stimulation of eukaryotic cells. Nature. 1985; 313(6002):481-4. DOI: 10.1038/313481a0. View

McNeil P, McKenna M, Taylor D . A transient rise in cytosolic calcium follows stimulation of quiescent cells with growth factors and is inhibitable with phorbol myristate acetate. J Cell Biol. 1985; 101(2):372-9. PMC: 2113666. DOI: 10.1083/jcb.101.2.372. View

Zachary I, Rozengurt E . High-affinity receptors for peptides of the bombesin family in Swiss 3T3 cells. Proc Natl Acad Sci U S A. 1985; 82(22):7616-20. PMC: 391384. DOI: 10.1073/pnas.82.22.7616. View

. Early changes in inositol lipids and their metabolites induced by platelet-derived growth factor in quiescent Swiss mouse 3T3 cells. Biochem J. 1985; 232(1):99-109. PMC: 1152845. DOI: 10.1042/bj2320099. View

MENDOZA S, Lopez-Rivas A, Rozengurt E . Phorbol esters and diacylglycerol inhibit vasopressin-induced increases in cytoplasmic-free Ca2+ and 45Ca2+ efflux in Swiss 3T3 cells. Exp Cell Res. 1986; 164(2):536-45. DOI: 10.1016/0014-4827(86)90051-0. View

10.

MENDOZA S, Schneider J, Lopez-Rivas A, Rozengurt E . Early events elicited by bombesin and structurally related peptides in quiescent Swiss 3T3 cells. II. Changes in Na+ and Ca2+ fluxes, Na+/K+ pump activity, and intracellular pH. J Cell Biol. 1986; 102(6):2223-33. PMC: 2114269. DOI: 10.1083/jcb.102.6.2223. View

11.

Rozengurt E, MENDOZA S . Synergistic signals in mitogenesis: role of ion fluxes, cyclic nucleotides and protein kinase C in Swiss 3T3 cells. J Cell Sci Suppl. 1985; 3:229-42. DOI: 10.1242/jcs.1985.supplement_3.20. View

12.

Meek J . Inositol bis-, tris-, and tetrakis(phosphate)s: analysis in tissues by HPLC. Proc Natl Acad Sci U S A. 1986; 83(12):4162-6. PMC: 323691. DOI: 10.1073/pnas.83.12.4162. View

13.

Ross R, Raines E, Bowen-Pope D . The biology of platelet-derived growth factor. Cell. 1986; 46(2):155-69. DOI: 10.1016/0092-8674(86)90733-6. View

14.

Rozengurt E . Early signals in the mitogenic response. Science. 1986; 234(4773):161-6. DOI: 10.1126/science.3018928. View

15.

Heslop J, Blakeley D, Brown K, Irvine R, Berridge M . Effects of bombesin and insulin on inositol (1,4,5)trisphosphate and inositol (1,3,4)trisphosphate formation in Swiss 3T3 cells. Cell. 1986; 47(5):703-9. DOI: 10.1016/0092-8674(86)90513-1. View

16.

MAJERUS P, Connolly T, Deckmyn H, Ross T, Bross T, Ishii H . The metabolism of phosphoinositide-derived messenger molecules. Science. 1986; 234(4783):1519-26. DOI: 10.1126/science.3024320. View

17.

Takuwa N, Takuwa Y, Bollag W, Rasmussen H . The effects of bombesin on polyphosphoinositide and calcium metabolism in Swiss 3T3 cells. J Biol Chem. 1987; 262(1):182-8. View

18.

Zachary I, Rozengurt E . Identification of a receptor for peptides of the bombesin family in Swiss 3T3 cells by affinity cross-linking. J Biol Chem. 1987; 262(9):3947-50. View

19.

Clapper D, Walseth T, Dargie P, Lee H . Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J Biol Chem. 1987; 262(20):9561-8. View

20.

Lopez-Rivas A, MENDOZA S, Nanberg E, Sinnett-Smith J, Rozengurt E . Ca2+-mobilizing actions of platelet-derived growth factor differ from those of bombesin and vasopressin in Swiss 3T3 mouse cells. Proc Natl Acad Sci U S A. 1987; 84(16):5768-72. PMC: 298944. DOI: 10.1073/pnas.84.16.5768. View