Contribution of gene-modified mice and rats to our understanding of the cardiovascular pharmacology of serotonin

Pharmacology and Therapeutics

Volumn 128, Issue 3, 2010, Pages 559-567

  Monassier, Laurent ^a,b   Laplante, Marc André ^a   Ayadi, Tarak ^a   Doly, Stéphane ^c   Maroteaux, Luc ^c  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT CLINIQUE DE LA SOURIS   (France)

^c INSTITUT DU FER À MOULIN   (France)

Author keywords

Cardiac hypertrophy; Cytokines; Development; Hemostasis; Hypertension; Pulmonary; Serotonin

Indexed keywords

1,2,3,5 TETRAHYDRO 5 METHYL 1 (3 PYRIDYLCARBAMOYL)PYRROLO[2,3 F]INDOLE; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; ANGIOTENSIN II; CYTOKINE; DIPYRIDAMOLE; ISOPRENALINE; KETANSERIN; LY 272015; NORADRENALIN; SB 215505; SEROTONIN; SEROTONIN 2 ANTAGONIST; SEROTONIN 2B RECEPTOR; SEROTONIN 4 RECEPTOR; SEROTONIN TRANSPORTER; TRYPTOPHAN HYDROXYLASE; UNCLASSIFIED DRUG;

BLOOD PRESSURE REGULATION; BLOOD VESSEL TONE; CARDIOVASCULAR EFFECT; CHRONIC HYPOXIA; CONGESTIVE CARDIOMYOPATHY; CYTOKINE RELEASE; EXPERIMENTAL MOUSE; EXPERIMENTAL RAT; FIBROBLAST; GENE OVEREXPRESSION; HEART; HEART CONDUCTION; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEMOSTASIS; HUMAN; HYPERTENSION; HYPOXIA; LUNG BLOOD VESSEL; LUNG FIBROSIS; MORPHOGENESIS; NONHUMAN; NORADRENALIN BLOOD LEVEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RECEPTOR GENE; REGULATORY MECHANISM; REVIEW; SEROTONINERGIC SYSTEM; THROMBOCYTE; THROMBOCYTE AGGREGATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOOD PLATELETS; CARDIOVASCULAR ABNORMALITIES; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; HEART; HEMOSTASIS; MICE; MICE, KNOCKOUT; RATS; RATS, MUTANT STRAINS; RECEPTOR, SEROTONIN, 5-HT1B; RECEPTORS, SEROTONIN; SEROTONIN;

EID: 78049316309     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2010.08.004     Document Type: Review

References (88)

1. Ahmed B.A., Jeffus B.C., Bukhari S.I.A., Harney J.T., Unal R., Lupashin V.V., van der Sluijs P., Kilic F. Serotonin transamidates Rab4 and facilitates its binding to the C terminus of serotonin transporter. J Biol Chem 2008, 283:9388-9398.
2. Angeles D.M., Williams J., Zhang L., Pearce W.J. Acute hypoxia modulates 5-HT receptor density and agonist affinity in fetal and adult ovine carotid arteries. Am J Physiol Heart Circ Physiol 2000, 279:H502-H510.
3. Angeles D.M., Williams J., Purdy R.E., Zhang L., Pearce W.J. Effects of maturation and acute hypoxia on receptor-IP(3) coupling in ovine common carotid arteries. Am J Physiol Regul Integr Comp Physiol 2001, 280:R410-R417.
4. 1B receptors during development of DOCA-salt hypertension. BMC Pharmacol 2003, 3:12.
5. Berul C.I., Christe M.E., Aronovitz M.J., et al. Familial hypertrophic cardiomyopathy mice display gender differences in electrophysiological abnormalities. J Interv Card Electrophysiol 1998, 2:7-14.
6. Bhat G.B., Block E.R. Hypoxia directly increases serotonin transport by porcine pulmonary artery endothelial cell plasma membrane vesicles. Am J Respir Cell Mol Biol 1990, 3:363-367.
7. Bianchi P., Kunduzova O., Masini E., Cambon C., Bani D., Raimondi L., Seguelas M.H., Nistri S., Colucci W., Leducq N., et al. Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 2005, 112:3297-3305.
8. Brune S., Schmidt T., Tebbe U., Kreuzer H. Influence of long-term treatment with ketanserin on blood pressure, pulmonary artery pressure, and cardiac output in patients with heart failure. Cardiovasc Drugs Ther Cardiovascular Pharmacotherapy 1990, 4(Suppl 1):85-87.
9. 2B receptors in mice. J Pharmacol Exp Ther 2006, 317:724-731.
10. Carneiro A.M., Cook E.H., Murphy D.L., Blakely R.D. Interactions between integrin alphaIIbbeta3 and the serotonin transporter regulate serotonin transport and platelet aggregation in mice and humans. J Clin Invest 2008, 118:1544-1552.
11. 2B receptor-mediated serotonin morphogenetic functions in mouse cranial neural crest and myocardiac cells. Development 1997, 124:1745-1755.
12. 2A receptor. J Neurochem 1994, 63:465-469.
13. Cote F., Fligny C., Bayard E., Launay J.M., Gershon M.D., Mallet J., Vodjdani G. Maternal serotonin is crucial for murine embryonic development. Proc Natl Acad Sci USA 2007, 104:329-334.
14. Côté F., Thevenot E., Fligny C., Fromes Y., Darmon M., Ripoche M.A., Bayard E., Hanoun N., Saurini F., Lechat P., et al. Disruption of the nonneuronal tph1 gene demonstrates the importance of peripheral serotonin in cardiac function. Proc Natl Acad Sci USA 2003, 100:13525-13530.
15. 2A receptor stimulation. J Pharmacol Exp Ther 2008, 326:153-162.
16. Dale G.L., Friese P., Batar P., Hamilton S.F., Reed G.L., Jackson K.W., Clemetson K.J., Alberio L. Stimulated platelets use serotonin to enhance their retention of procoagulant proteins on the cell surface. Nature 2002, 415:175-179.
17. 1D autoreceptors. Neuropharmacology 1996, 35:1627-1634.
18. Eddahibi S., Fabre V., Boni C., Martres M.P., Raffestin B., Hamon M., Adnot S. Induction of serotonin transporter by hypoxia in pulmonary vascular smooth muscle cells. Relationship with the mitogenic action of serotonin. Circ Res 1999, 84:329-336.
19. Eddahibi S., Hanoun N., Lanfumey L., Lesch K.P., Raffestin B., Hamon M., Adnot S. Attenuated hypoxic pulmonary hypertension in mice lacking the 5-hydroxytryptamine transporter gene. J Clin Invest 2000, 105:1555-1562.
20. Esteve J.M., Launay J.M., Kellermann O., Maroteaux L. Functions of serotonin in hypoxic pulmonary vascular remodeling. Cell Biochem Biophys 2007, 47:33-44.
21. Fanburg B.L., Lee S.L. A role for the serotonin transporter in hypoxia-induced pulmonary hypertension. J Clin Invest 2000, 105:1521-1523.
22. Farber H.W., Loscalzo J. Pulmonary arterial hypertension. N Engl J Med 2004, 351:1655-1665.
23. Fligny C., Fromes Y., Bonnin P., Darmon M., Bayard E., Launay J.M., Cote F., Mallet J., Vodjdani G. Maternal serotonin influences cardiac function in adult offspring. FASEB J 2008, 22:2340-2349.
24. Fu X.W., Nurse C.A., Wong V., Cutz E. Hypoxia-induced secretion of serotonin from intact pulmonary neuroepithelial bodies in neonatal rabbit. J Physiol 2002, 539:503-510.
25. Guilluy C., Rolli-Derkinderen M., Tharaux P.L., Melino G., Pacaud P., Loirand G. Transglutaminase-dependent RhoA activation and depletion by serotonin in vascular smooth muscle cells. J Biol Chem 2007, 282:2918-2928.
26. Guilluy C., Eddahibi S., Agard C., Guignabert C., Izikki M., Tu L., Savale L., Humbert M., Fadel E., Adnot S., et al. RhoA and Rho kinase activation in human pulmonary hypertension: role of 5-HT signaling. Am J Respir Crit Care Med 2009, 179:1151-1158.
27. Herve P., Drouet L., Dosquet C., Launay J.M., Rain B., Simonneau G., Caen J., Duroux P. Primary pulmonary hypertension in a patient with a familial platelet storage pool disease: role of serotonin. Am J Med 1990, 89:117-120.
28. Herve P., Launay J.M., Scrobohaci M.L., Brenot F., Simonneau G., Petitpretz P., Poubeau P., Cerrina J., Duroux P., Drouet L. Increased plasma serotonin in primary pulmonary hypertension. Am J Med 1995, 99:249-254.
29. Homberg J., Mudde J., Braam B., Ellenbroek B., Cuppen E., Joles J.A. Blood pressure in mutant rats lacking the 5-hydroxytryptamine transporter. Hypertension 2006, 48:e115-e116.
30. Homberg J.R., Pattij T., Janssen M.C., Ronken E., De Boer S.F., Schoffelmeer A.N., Cuppen E. Serotonin transporter deficiency in rats improves inhibitory control but not behavioural flexibility. Eur J Neurosci 2007, 26:2066-2073.
31. 1Beta, and tumor necrosis factor-alpha cytokine production by ventricular fibroblasts. Circulation 2004, 110:969-974.
32. Jaffre F., Bonnin P., Callebert J., Debbabi H., Setola V., Doly S., Monassier L., Mettauer B., Blaxall B.C., Launay J.M., et al. Serotonin and angiotensin receptors in cardiac fibroblasts coregulate adrenergic-dependent cardiac hypertrophy. Circ Res 2009, 104:113-123.
33. Jeffery T.K., Wanstall J.C. Pulmonary vascular remodeling: a target for therapeutic intervention in pulmonary hypertension. Pharmacol Ther 2001, 92:1-20.
34. Jonnakuty C., Gragnoli C. What do we know about serotonin?. J Cell Physiol 2008, 217(2):301-306.
35. Kamel R., Garcia S., Lezoualc'h F., Fischmeister R., Muller S., Hoebek J., Eftekhari P. Immunomodulation by maternal autoantibodies of the fetal serotoninergic 5-HT4 receptor and its consequences in early BALB/c mouse embryonic development. BMC Dev Biol 2007, 7:34.
36. 1B/1D)-receptor antagonist GR127935. Circ Res 2001, 89:1231-1239.
37. Keith I.M., Will J.A., Huxtable R.J., Weir K. Anti-platelet agents reduce morphological changes of chronic hypoxic pulmonary hypertension. Histol Histopathol 1987, 2:203-206.
38. Kentera D., Susic D., Veljkovic V., Tucakovic G., Koko V. Pulmonary artery pressure in rats with hereditary platelet function defect. Respiration 1988, 54:110-114.
39. Kereveur A., Callebert J., Humbert M., Herve P., Simonneau G., Launay J.M., Drouet L. High plasma serotonin levels in primary pulmonary hypertension. Effect of long-term epoprostenol (prostacyclin) therapy. Arterioscler Thromb Vasc Biol 2000, 20:2233-2239.
40. Kirby G.C., McQueen D.S. Effects of the antagonists MDL 72222 and ketanserin on responses of cat carotid body chemoreceptors to 5-hydroxytryptamine. Br J Pharmacol 1984, 83:259-269.
41. Lairez O., Calise D., Bianchi P., Ordener C., Spreux-Varoquaux O., Guilbeau-Frugier C., Escourrou G., Seif I., Roncalli J., Pizzinat N., et al. Genetic deletion of MAO-A promotes serotonin-dependent ventricular hypertrophy by pressure overload. J Mol Cell Cardiol 2009, 46:587-595.
42. 2C) receptors in the mouse embryo. Int J Dev Neurosci 2000, 18:653-662.
43. 2B receptor controls the overall 5-HT transport system in the 1C11 serotonergic cell line. Ann NY Acad Sci 1998, 861:247.
44. 2B receptor in pulmonary hypertension. Nat Med 2002, 8:1129-1135.
45. Lee S.L., Wang W.W., Moore B.J., Fanburg B.L. Dual effect of serotonin on growth of bovine pulmonary artery smooth muscle cells in culture. Circ Res 1991, 68:1362-1368.
46. Li N., Wallen N.H., Ladjevardi M., Hjemdahl P. Effects of serotonin on platelet activation in whole blood. Blood Coagul Fibrinolysis 1997, 8:517-523.
47. Linder A.E., Ni W., Szasz T., Burnett R., Diaz J., Geddes T.J., Kuhn D.M., Watts S.W. A serotonergic system in veins: serotonin transporter-independent uptake. J Pharmacol Exp Ther 2008, 325:714-722.
48. MacLean M.R., Deuchar G.A., Hicks M.N., Morecroft I., Shen S., Sheward J., Colston J., Loughlin L., Nilsen M., Dempsie Y., et al. Overexpression of the 5-hydroxytryptamine transporter gene: effect on pulmonary hemodynamics and hypoxia-induced pulmonary hypertension. Circulation 2004, 109:2150-2155.
49. Marcos E., Adnot S., Pham M.H., Nosjean A., Raffestin B., Hamon M., Eddahibi S. Serotonin transporter inhibitors protect against hypoxic pulmonary hypertension. Am J Respir Crit Care Med 2003, 168:487-493.
50. Matondo R.B., Punt C., Homberg J., Toussaint M.J., Kisjes R., Korporaal S.J., Akkerman J.W., Cuppen E., de Bruin A. Deletion of the serotonin transporter in rats disturbs serotonin homeostasis without impairing liver regeneration. Am J Physiol Gastrointest Liver Physiol 2009, 296:G963-G968.
51. McDonald T.P., Cottrell M., Clift R. Effects of short-term hypoxia on platelet counts of mice. Blood 1978, 51:165-175.
52. McDonald T.P., Cottrell M.B., Steward S.A., Clift R.E., Swearingen C.J., Jackson C.W. Comparison of platelet production in two strains of mice with different modal megakaryocyte DNA ploidies after exposure to hypoxia. Exp Hematol 1992, 20:51-56.
53. Mekontso-Dessap A., Brouri F., Pascal O., Lechat P., Hanoun N., Lanfumey L., Seif I., Benhaiem-Sigaux N., Kirsch M., Hamon M., et al. Deficiency of the 5-hydroxytryptamine transporter gene leads to cardiac fibrosis and valvulopathy in mice. Circulation 2006, 113:81-89.
54. 2B) receptor blockade prevents reactive oxygen species-induced cardiac hypertrophy in mice. Hypertension 2008, 52:301-307.
55. Morecroft I., Loughlin L., Nilsen M., Colston J., Dempsie Y., Sheward J., Harmar A., MacLean M.R. Functional interactions between 5-hydroxytryptamine receptors and the serotonin transporter in pulmonary arteries. J Pharmacol Exp Ther 2005, 313:539-548.
56. Morecroft I., Dempsie Y., Bader M., Walther D.J., Kotnik K., Loughlin L., Nilsen M., MacLean M.R. Effect of tryptophan hydroxylase 1 deficiency on the development of hypoxia-induced pulmonary hypertension. Hypertension 2007, 49:232-236.
57. 2B) receptors in mice leads to abnormal cardiac structure and function. Circulation 2001, 103:2973-2979.
58. 2B receptor in heart leads to abnormal mitochondrial function and cardiac hypertrophy. Circulation 2003, 107:3223-3229.
59. Ni W., Wilhelm C.S., Bader M., Murphy D.L., Lookingland K., Watts S.W. (+)-Norfenfluramine-induced arterial contraction is not dependent on endogenous 5-hydroxytryptamine or 5-hydroxytryptamine transporter. J Pharmacol Exp Ther 2005, 314:953-960.
60. Ni W., Geddes T.J., Priestley J.R., Szasz T., Kuhn D.M., Watts S.W. The existence of a local 5-hydroxytryptaminergic system in peripheral arteries. Br J Pharmacol 2008, 154:663-674.
61. Paulmann N., Grohmann M., Voigt J.-P., Bert B., Vowinckel J., Bader M., Skelin M., Jevsek M., Fink H., Rupnik M., et al. Intracellular serotonin modulates insulin secretion from pancreatic beta-cells by protein serotonylation. PLoS Biol 2009, 7:e1000229.
62. Pavone L.M., Mithbaokar P., Mastellone V., Avallone L., Gaspar P., Maharajan V., Baldini A. Fate map of serotonin transporter-expressing cells in developing mouse heart. Genesis 2007, 45:689-695.
63. Pavone L.M., Spina A., Lo Muto R., Santoro D., Mastellone V., Avallone L. Heart valve cardiomyocytes of mouse embryos express the serotonin transporter SERT. Biochem Biophys Res Commun 2008, 377:419-422.
64. Pitt B.R., Weng W., Steve A.R., Blakely R.D., Reynolds I., Davies P. Serotonin increases DNA synthesis in rat proximal and distal pulmonary vascular smooth muscle cells in culture. Am J Physiol 1994, 266:L178-L186.
65. Qvigstad E., Brattelid T., Sjaastad I., Andressen K.W., Krobert K.A., Birkeland J.A., Sejersted O.M., Kaumann A.J., Skomedal T., Osnes J.B., et al. Appearance of a ventricular 5-HT4 receptor-mediated inotropic response to serotonin in heart failure. Cardiovasc Res 2005, 65(4):869-878.
66. Rabinovitch M. Linking a serotonin transporter polymorphism to vascular smooth muscle proliferation in patients with primary pulmonary hypertension. J Clin Invest 2001, 108:1109-1111.
67. Rapport M.M., Green A.A., Page I.H. Crystalline serotonin. Science 1948, 108:329-330.
68. Rapport M.M., Green A.A., Page I.H. Serum vasoconstrictor, serotonin; isolation and characterization. J Biol Chem 1948, 176:1243-1251.
69. Reeves J.T., Groves B.M., Turkevich D. The case for treatment of selected patients with primary pulmonary hypertension. Am Rev Respir Dis 1986, 134:342-346.
70. Robiolio P.A., Rigolin V.H., Wilson J.S., Harrison J.K., Sanders L.L., Bashore T.M., Feldman J.M. Carcinoid heart disease. Correlation of high serotonin levels with valvular abnormalities detected by cardiac catheterization and echocardiography. Circulation 1995, 92:790-795.
71. Rostagno C., Prisco D., Boddi M., Poggesi L. Evidence for local platelet activation in pulmonary vessels in patients with pulmonary hypertension secondary to chronic obstructive pulmonary disease. Eur Respir J 1991, 4:147-151.
72. Roux C., Madani M., Launay J.-M., Rey F., Citadelle D., Mulliez N., Kolf M. Serotonin deficiency in phenylketonuria embryopathy. Toxicol in Vitro 1995, 9:653-662.
73. Sanchez C., Hyttel J. Comparison of the effects of antidepressants and their metabolites on reuptake of biogenic amines and on receptor binding. Cell Mol Neurobiol 1999, 19:467-489.
74. Sato K., Webb S., Tucker A., Rabinovitch M., O'Brien R.F., McMurtry I.F., Stelzner T.J. Factors influencing the idiopathic development of pulmonary hypertension in the fawn hooded rat. Am Rev Respir Dis 1992, 145:793-797.
75. Setola V., Roth B.L. Why mice are neither miniature humans nor small rats: a cautionary tale involving 5-hydroxytryptamine-6 serotonin receptor species variants. Mol Pharmacol 2003, 64:1277-1278.
76. Steele P., Ellis J.H., Weily H.S., Genton E. Platelet survival time in patients with hypoxemia and pulmonary hypertension. Circulation 1977, 55:660-661.
77. Tolmachova T., Abrink M., Futter C.E., Authi K.S., Seabra M.C. Rab27b regulates number and secretion of platelet dense granules. Proc Natl Acad Sci USA 2007, 104:5872-5877.
78. Tournois C., Mutel V., Manivet P., Launay J.M., Kellermann O. Cross-talk between 5-hydroxytryptamine receptors in a serotonergic cell line. Involvement of arachidonic acid metabolism. J Biol Chem 1998, 273:17498-17503.
79. Tu D.N., Zou A.R., Liao Y.H., Du Y.M., Wang X.P., Li L. Blockade of the human ether-a-go-go-related gene potassium channel by ketanserin. Sheng Li Xue Bao 2008, 60:525-534.
80. Vane J.R. A sensitive method for the assay of 5-hydroxytryptamine. Br J Pharmacol Chemother 1957, 12:344-349.
81. Vially M., Erspamer V. Cellule entreocromaffine e cellule basigranulose acidofile nei vertebrati. Zeitschr f Zellforsch 1933, 19:743-773.
82. Vyssoulis G.P., Karpanou E.A., Pitsavos C.E., Paleologos A.A., Kourtis T.K., Toutouzas P.K. Left ventricular hypertrophy regression and function changes with ketanserin in elderly hypertensives. Cardiovasc Drugs Ther 1990, 4:81-84.
83. Walther D.J., Peter J.U., Winter S., Holtje M., Paulmann N., Grohmann M., Vowinckel J., Alamo-Bethencourt V., Wilhelm C.S., Ahnert-Hilger G., et al. Serotonylation of small GTPases is a signal transduction pathway that triggers platelet alpha-granule release. Cell 2003, 115:851-862.
84. Wanstall J.C., Fiore S.A., Gambino A., Chess-Williams R. Potentiation of 5-hydroxytryptamine (5-HT) responses by a 5-HT uptake inhibitor in pulmonary and systemic vessels: effects of exposing rats to hypoxia. Naunyn Schmiedebergs Arch Pharmacol 2003, 368(6):520-527.
85. Watts S.W. The love of a lifetime: 5-HT in the cardiovascular system. Am J Physiol Regul Integr Comp Physiol 2009, 296:R252-R256.
86. Watts S.W., Priestley J.R.C., Thompson J.M. Serotonylation of vascular proteins important to contraction. PLoS ONE 2009, 4:e5682.
87. Weiss, O. (1896). Über die Wirkungen von Blutserum-Injectionen ins Blut. Archiv für die Gesamte Physiologie des Menschen und der Thiere LXV, 215-230.
88. Woulfe D.S., Lilliendahl J.K., August S., Rauova L., Kowalska M.A., Abrink M., Pejler G., White J.G., Schick B.P. Serglycin proteoglycan deletion induces defects in platelet aggregation and thrombus formation in mice. Blood 2008, 111:3458-3467.