Maturational Regulation of Inositol 1,4,5-trisphosphate Metabolism in Rabbit Airway Smooth Muscle

Overview

Journal J Clin Invest

Specialty General Medicine

Date 1991 Dec 1

PMID 1661295

Citations 4

Authors

S M ROSENBERG

G T Berry

J R Yandrasitz

M M Grunstein

Affiliations

Soon will be listed here.

Abstract

Airway reactivity has been shown to vary with age; however, the mechanism(s) underlying this process remain unidentified. To elucidate the role of ontogenetic changes in phosphoinositide-linked signal transduction, we examined whether age-related differences in tracheal smooth muscle (TSM) contractility to carbachol (CCh) are associated with developmental changes in the production and metabolism of the second messenger, inositol 1,4,5-trisphosphate (Ins (1,4,5)P3). In TSM segments isolated from 2-wk-old and adult rabbits, both the maximal isometric contractile force and sensitivity (i.e., -logED50) to CCh (10(-10)-10(-4) M) were significantly greater in the immature vs. adult tissues (P less than 0.001). Similarly, Ins(1,4,5)P3 accumulation elicited by either receptor-coupled stimulation with CCh (10(-10)-10(-4) M) or post-receptor-mediated guanine nucleotide binding protein activation of permeabilized TSM with GTP gamma S (100 microM) was also significantly enhanced in 2-wk-old vs. adult TSM. Measurement of the activities of the degradative enzymes for Ins(1,4,5)P3 demonstrated that: (a) mean +/- SE maximal Ins(1,4,5)P3 3'-kinase activity was significantly reduced in the immature vs. adult TSM (i.e., approximately 71.7 +/- 6.0 vs. 137.8 +/- 10.0 pmol/min per mg protein, respectively; P less than 0.005); (b) by contrast, maximal Ins(1,4,5)P3 5'-phosphatase activity was significantly increased in the immature vs. adult TSM (i.e., 27.9 +/- 1.2 vs. 15.6 +/- 1.5 nmol/min per mg protein, respectively; P less than 0.001); and (c) the Km values for Ins(1,4,5)P3 5'-phosphatase were 14- and 19-fold greater than those for Ins(1,4,5)P3 3'-kinase in the 2-wk-old and adult TSM, respectively. Collectively, the findings suggest that the age-related decrease in agonist-induced rabbit TSM contractility is associated with a diminution in Ins(1,4,5)P3 accumulation which is attributed, at least in part, to ontogenetic changes in the relative activities of the degradative enzymes for Ins(1,4,5)P3.

Citing Articles

Ontogenesis of myosin light chain kinase mRNA and protein content in guinea pig tracheal smooth muscle.

Chitano P, Voynow J, Pozzato V, Cantillana V, Burch L, Wang L Pediatr Pulmonol. 2004; 38(6):456-64.

PMID: 15376333 PMC: 2527445. DOI: 10.1002/ppul.20118.

Muscarinic regulation of cytosolic free calcium in canine tracheal smooth muscle cells: Ca2+ requirement for phospholipase C activation.

Yang C, Chou S, Wang Y, Hsieh J, Ong R Br J Pharmacol. 1993; 110(3):1239-47.

PMID: 8298814 PMC: 2175810. DOI: 10.1111/j.1476-5381.1993.tb13948.x.

5-Hydroxytryptamine receptor-mediated phosphoinositide hydrolysis in canine cultured tracheal smooth muscle cells.

Yang C, Yo Y, Hsieh J, Ong R Br J Pharmacol. 1994; 111(3):777-86.

PMID: 8019756 PMC: 1910084. DOI: 10.1111/j.1476-5381.1994.tb14805.x.

Bradykinin-stimulated phosphoinositide metabolism in cultured canine tracheal smooth muscle cells.

Yang C, Hsia H, Chou S, Ong R, Hsieh J, Luo S Br J Pharmacol. 1994; 111(1):21-8.

PMID: 8012698 PMC: 1910033. DOI: 10.1111/j.1476-5381.1994.tb14018.x.

References

Kitazawa T, Kobayashi S, Horiuti K, Somlyo A, Somlyo A . Receptor-coupled, permeabilized smooth muscle. Role of the phosphatidylinositol cascade, G-proteins, and modulation of the contractile response to Ca2+. J Biol Chem. 1989; 264(10):5339-42. View

Hayashi S, Toda N . Age-related alterations in the response of rabbit tracheal smooth muscle to agents. J Pharmacol Exp Ther. 1980; 214(3):675-81. View

Yamaguchi K, Hirata M, Kuriyama H . Calmodulin activates inositol 1,4,5-trisphosphate 3-kinase activity in pig aortic smooth muscle. Biochem J. 1987; 244(3):787-91. PMC: 1148065. DOI: 10.1042/bj2440787. View

Miller-Hance W, Miller J, Wells J, Stull J, Kamm K . Biochemical events associated with activation of smooth muscle contraction. J Biol Chem. 1988; 263(28):13979-82. View

Montgomery G, Tepper R . Changes in airway reactivity with age in normal infants and young children. Am Rev Respir Dis. 1990; 142(6 Pt 1):1372-6. DOI: 10.1164/ajrccm/142.6_Pt_1.1372. View

Grunstein M, ROSENBERG S, Schramm C, Pawlowski N . Mechanisms of action of endothelin 1 in maturing rabbit airway smooth muscle. Am J Physiol. 1991; 260(6 Pt 1):L434-43. DOI: 10.1152/ajplung.1991.260.6.L434. View

MURRAY R, Bennett C, Fluharty S, Kotlikoff M . Mechanism of phorbol ester inhibition of histamine-induced IP3 formation in cultured airway smooth muscle. Am J Physiol. 1989; 257(4 Pt 1):L209-16. DOI: 10.1152/ajplung.1989.257.4.L209. View

Huang C, IVES H . Guanosine 5'-O-(3-thiotrisphosphate) potentiates both thrombin- and platelet-derived growth factor-induced inositol phosphate release in permeabilized vascular smooth muscle cells. Signaling mechanisms distinguished by sensitivity to pertussis toxin.... J Biol Chem. 1989; 264(8):4391-7. View

Connolly T, Lawing Jr W, MAJERUS P . Protein kinase C phosphorylates human platelet inositol trisphosphate 5'-phosphomonoesterase, increasing the phosphatase activity. Cell. 1986; 46(6):951-8. DOI: 10.1016/0092-8674(86)90077-2. View

10.

Abdel-Latif A . Calcium-mobilizing receptors, polyphosphoinositides, and the generation of second messengers. Pharmacol Rev. 1986; 38(3):227-72. View

11.

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

12.

Balduini W, Murphy S, Costa L . Developmental changes in muscarinic receptor-stimulated phosphoinositide metabolism in rat brain. J Pharmacol Exp Ther. 1987; 241(2):421-7. View

13.

Biden T, Comte M, Cox J, Wollheim C . Calcium-calmodulin stimulates inositol 1,4,5-trisphosphate kinase activity from insulin-secreting RINm5F cells. J Biol Chem. 1987; 262(20):9437-40. View

14.

Chilvers E, Challiss R, Barnes P, Nahorski S . Mass changes of inositol(1,4,5)trisphosphate in trachealis muscle following agonist stimulation. Eur J Pharmacol. 1989; 164(3):587-90. DOI: 10.1016/0014-2999(89)90269-0. View

15.

Shears S . Metabolism of the inositol phosphates produced upon receptor activation. Biochem J. 1989; 260(2):313-24. PMC: 1138671. DOI: 10.1042/bj2600313. View

16.

Moon K, Lee S, Rhee S . Developmental changes in the activities of phospholipase c, 3-kinase, and 5-phosphatase in rat brain. Biochem Biophys Res Commun. 1989; 164(1):370-4. DOI: 10.1016/0006-291x(89)91728-2. View

17.

Kobayashi S, Kitazawa T, Somlyo A, Somlyo A . Cytosolic heparin inhibits muscarinic and alpha-adrenergic Ca2+ release in smooth muscle. Physiological role of inositol 1,4,5-trisphosphate in pharmacomechanical coupling. J Biol Chem. 1989; 264(30):17997-8004. View

18.

Murphy T, Mitchell R, Blake J, Mack M, Kelly E, Munoz N . Expression of airway contractile properties and acetylcholinesterase activity in swine. J Appl Physiol (1985). 1989; 67(1):174-80. DOI: 10.1152/jappl.1989.67.1.174. View

19.

MAJERUS P, Connolly T, Bansal V, Inhorn R, Ross T, Lips D . Inositol phosphates: synthesis and degradation. J Biol Chem. 1988; 263(7):3051-4. View

20.

Wills M, Douglas J . Aging and cholinergic responses in bovine trachealis muscle. Br J Pharmacol. 1988; 93(4):918-24. PMC: 1853884. DOI: 10.1111/j.1476-5381.1988.tb11480.x. View