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Angiotensin II stimulates arachidonic acid release from bone marrow stromal cells
Renee S Richmond
Hypertension and Vascular Disease Center Wake Forest University School of Medicine Winston-Salem, NC, USA
E Ann Tallant
Hypertension and Vascular Disease Center Wake Forest University School of Medicine Winston-Salem, NC, USA
Patricia E Gallagher
Hypertension and Vascular Disease Center Wake Forest University School of Medicine Winston-Salem, NC, USA
Carlos M Ferrario
Hypertension and Vascular Disease Center Wake Forest University School of Medicine Winston-Salem, NC, USA
William B Strawn
Hypertension and Vascular Disease Center Wake Forest University School of Medicine Winston-Salem, NC, USA, bstrawn{at}wfubmc.edu
Introduction Angiotensin II (Ang II) is recognised as a regulator of haematopoiesis, but its actions within the bone marrow are not fully understood. Support of haematopoiesis by bone marrow stromal cells (MSC) is dependent on factors that include arachidonic acid and macrophage colony stimulating factor (MCSF), both of which are increased by Ang II stimulation in other tissues. To further elucidate the mechanisms of Ang II-regulated haematopoiesis, we determined whether Ang II-stimulation alters arachidonic acid release and MCSF secretion from MSC.
Methods Cynomolgus monkey MSC isolated from bone marrow aspirates and the human HS-5 stromal cell line were studied for Ang II-mediated arachidonic acid (AA) release, while secretion of MCSF in response to Ang II was studied in HS-5 cells. Cells were labelled overnight with 3H-AA and the release of 3H-AA was measured in culture medium following 20 minutes stimulation with Ang II, alone or in combination with the AT1- or AT 2-receptor antagonists, losartan and PD 123319, respectively. MCSF secretion into culture medium was measured using an enzyme immunoassay following 24 hours of treatment with Ang II alone or in combination with losartan or PD 123319. Phorbol-myristate-acetate, known to stimulate release of AA and MCSF, was used as a positive control in both experiments.
Results In response to Ang II, release of 3H-AA from monkey and human MSC was increased (p<0.05) to 147±4% and 124±3% of control, respectively. The AT1- and AT2-receptor antagonists, losartan and PD 123319, individually reduced Ang II-stimulated 3H-AA release. In contrast, Ang II had no effect on secretion of MCSF from HS-5 cells.
Conclusions These results provide mechanistic evidence for Ang II-mediated haematopoiesis through AA release that may, in part, explain Ang II-facilitated recovery of haematopoiesis in experimental myelosuppression and the anaemias associated with Ang II receptor blockade.
Key Words: angiotensin II arachidonic acid marrow stromal haematopoiesis
References
- Haznedaroglu IC, Ozturk MA Towards the understanding of the local hematopoietic bone marrow renin-angiotensin system. Int J Biochem Cell Biol 2003;35:867-80.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Marathias KP, Agroyannis B., Mavromoustakos T., Matsoukas J., Vlahakos DV Hematocrit-lowering effect following inactivation of renin-angiotensin system with angiotensin converting enzyme inhibitors and angiotensin receptor blockers. Curr Top Med Chem 2004;4:483-6.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Cole J., Ertoy D., Lin H. et al. Lack of angiotensin II-facilitated erythropoiesis causes anemia in angiotensin-converting enzyme-deficient mice. J Clin Invest 2000;106:1391-8.[Web of Science][Medline]
[Order article via Infotrieve]
- Chisi JE, Wdzieczak-Bakala J., Thierry J., Briscoe CV, Riches AC Captopril inhibits the proliferation of hematopoietic stem and progenitor cells in murine long-term bone marrow cultures. Stem Cells 1999;17:339-44.[Web of Science][Medline]
[Order article via Infotrieve]
- Sica DS Pharmacotherapy in congestive heart failure:ACE inhibitors and anemia in congestive heart failure. Congest Heart Fail 2000;6:330-2.[CrossRef][Medline]
[Order article via Infotrieve]
- Ducloux D., Saint-Hillier Y., Chalopin JM Effect of losartan on haemoglobin concentration in renal transplant recipients-a retrospective analysis. Nephrol Dial Transplant 1997;12:2683-6.[Abstract/Free Full Text]
- Comte L., Lorgeot V., Volkov L., Allegraud A., Aldigier JC, Praloran V. Effects of the angiotensin-converting enzyme inhibitor enalapril on blood haematopoietic progenitors and acetyl-N-Ser-Asp-Lys-Pro concentrations. Eur J Clin Invest 1997;27:788-90.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Mukoyama M., Nakajima M., Horiuchi M., Sasamura H., Pratt RE, Dzau VJ Expression cloning of type 2 angiotensin II receptor reveals a unique class of seven-transmembrane receptors. J Biol Chem 1993;268:24539-42.[Abstract/Free Full Text]
- Kambayashi Y., Bardhan S., Takahashi K. et al. Molecular cloning of a novel angiotensin II receptor isoform involved in phosphotyrosine phosphatase inhibition. J Biol Chem 1993;268:24543-6.[Abstract/Free Full Text]
- Nishida M., Fujinaka H., Matsusaka T. et al. Absence of angiotensin II type 1 receptor in bone marrow-derived cells is detrimental in the evolution of renal fibrosis. J Clin Invest 2002;110:1859-68.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Gupta M., Miller BA, Ahsan N. et al. Expression of angiotensin II type I receptor on erythroid progenitors of patients with post transplant erythrocytosis. Transplantation 2000;70:1188-94.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Rodgers KE, Xiong S., diZerega GS Accelerated recovery from irradiation injury by angiotensin peptides. Cancer Chemother Pharmacol 2002;49:403-11.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Rodgers K., Xiong S., diZerega GS Effect of angiotensin II and angiotensin(1-7) on hematopoietic recovery after intravenous chemotherapy. Cancer Chemother Pharmacol 2003;51:97-106.[Web of Science][Medline]
[Order article via Infotrieve]
- Charrier S., Michaud A., Badaoui S. et al. Inhibition of Angiotensin I-converting enzyme induces radioprotection by preserving murine hematopoietic short-term reconstituting cells. Blood 2004;104:978-85.[Abstract/Free Full Text]
- Rodgers KE, Xiong S., Steer R., diZerega GS Effect of angiotensin II on hematopoietic progenitor cell proliferation. Stem Cells 2000;18:287-94.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Mrug M., Stopka T., Julian BA, Prchal JF, Prchal JT Angiotensin II stimulates proliferation of normal early erythroid progenitors. J Clin Invest 1997;100:2310-14.[Web of Science][Medline]
[Order article via Infotrieve]
- Strawn WB, Richmond RS, Ann TE, Gallagher PE, Ferrario CM Renin-angiotensin system expression in rat bone marrow haematopoietic and stromal cells. Br J Haematol 2004; 126:120-6.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Dorshkind K. Regulation of hemopoiesis by bone marrow stromal cells and their products. Annu Rev Immunol 1990; 8:111-37.[Web of Science][Medline]
[Order article via Infotrieve]
- Weiss L., Sakai H. The hematopoietic stroma. Am J Anat 1984;170:447-63.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Prasad A., Koh KK, Schenke WH et al. Role of angiotensin II type 1 receptor in the regulation of cellular adhesion molecules in atherosclerosis. Am Heart J 2001;142:248-53.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Torok-Storb B., Iwata M., Graf L., Gianotti J., Horton H., Byrne MC Dissecting the marrow microenvironment. Ann NY Acad Sci 1999;872:164-70.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Rizzo MT The role of arachidonic acid in normal and malignant haematopoiesis. Prostaglandins Leukot Essent Fatty Acids 2002;66:57-69.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Muthalif MM, Benter IF, Uddin MR, Harper JL, Malik KU Signal transduction mechanisms involved in angiotensin-(1-7)-stimulated arachidonic acid release and prostanoid synthesis in rabbit aortic smooth muscle cells. J Pharmacol Exp Ther 1998;284:388-98.[Abstract/Free Full Text]
- Lokuta AJ, Cooper C., Gaa ST, Wang HE, Rogers TB Angiotensin II stimulates the release of phospholipid-derived second messengers through multiple receptor subtypes in heart cells. JBiol Chem 1994;269:4832-8.[Abstract/Free Full Text]
- Zhu M., Gelband CH, Moore JM, Posner P., Sumners C. Angiotensin II type 2 receptor stimulation of neuronal delayed-rectifier potassium current involves phospholipase A2 and arachidonic acid. J Neurosci 1998;18:679-86.[Abstract/Free Full Text]
- Takai S., Kim S., Sakonjo H., Miyazaki M. Mechanisms of angiotensin II type 1 receptor blocker for anti-atherosclerotic effect in monkeys fed a high-cholesterol diet. J Hypertens 2003;21:361-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Sadamatsu K., Shimokawa H.,Tashiro H., Yamamoto K. Long term treatment with enalapril reduces plasma concentrations of macrophage colony stimulating factor in patients with coronary artery disease. Heart 2001;86:457-8.[Free Full Text]
- de Revel T., Becard N., Sorg T. et al. Retroviral interleukin 1alpha gene transfer in bone marrow stromal cells in a primate model: induction of myelopoiesis stimulation. Br J Haematol 2002;118:875-84.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Strawn WB, Chappell MC, Dean RH, Kivlighn S., Ferrario CM Inhibition of early atherogenesis by losartan in monkeys with diet-induced hypercholesterolemia. Circulation 2000; 101:1586-93.[Abstract/Free Full Text]
- Roecklein BA,Torok-Storb B. Functionally distinct human marrow stromal cell lines immortalized by transduction with the human papilloma virus E6/E7 genes. Blood 1995;85:997-1005.[Abstract/Free Full Text]
- Dulin NO,Alexander LD, Harwalkar S., Falck JR, Douglas JG Phospholipase A2-mediated activation of mitogen-activated protein kinase by angiotensin II. Proc Natl Acad Sci U S A 1998;95:8098-102.[Abstract/Free Full Text]
- Birbes H., Pageaux JF, Fayard JM, Lagarde M., Laugier C. Protein kinase C inhibitors stimulate arachidonic and docosahexaenoic acids release from uterine stromal cells through a Ca2+-independent pathway. FEBS Lett 1998;432:219-24.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Doerfler ME, Weiss J., Clark JD, Elsbach P. Bacterial lipopolysaccharide primes human neutrophils for enhanced release of arachidonic acid and causes phosphorylation of an 85-kD cytosolic phospholipase A2. J Clin Invest 1994;93:1583-91.[Web of Science][Medline]
[Order article via Infotrieve]
- Qiu ZH, de Carvalho MS, Leslie CC Regulation of phospholipase A2 activation by phosphorylation in mouse peritoneal macrophages. J Biol Chem 1993;268:24506-13.[Abstract/Free Full Text]
- Lemieux LI, Rahal SS, Kennedy CR PGE2 reduces arachidonic acid release in murine podocytes; evidence for an autocrine feedback loop. Am J Physiol Cell Physiol 2003; 284:C302-C309.[Abstract/Free Full Text]
- Kicic A., Shanley AC, Hall CM, Rakoczy PE Marrow stromal cells (MSC): a species comparison. Adv Exp Med Biol 2003;533:407-14.[Web of Science][Medline]
[Order article via Infotrieve]
- Woodbury D., Schwarz EJ, Prockop DJ, Black IB Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000;61:364-70.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Suva D., Garavaglia G., Menetrey J. et al. Non-hematopoietic human bone marrow contains long-lasting, pluripotential mesenchymal stem cells. J Cell Physiol 2004;198:110-18.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Fixe P., Rougier F., Ostyn E. et al. Spontaneous and inducible production of macrophage colony-stimulating factor by human bone marrow stromal cells. Eur Cytokine Netw 1997;8:91-5.[Web of Science][Medline]
[Order article via Infotrieve]
- Nahmod KA,Vermeulen ME, Raiden S. et al. Control of dendritic cell differentiation by angiotensin II. FASEB J 2003; 17:491-3.[Abstract/Free Full Text]
- Mifune M., Sasamura H., Shimizu-Hirota R., Miyazaki H., Saruta T. Angiotensin II type 2 receptors stimulate collagen synthesis in cultured vascular smooth muscle cells. Hypertension 2000;36:845-50.[Abstract/Free Full Text]
- Moriguchi Y., Matsubara H., Mori Y. et al. Angiotensin IIinduced transactivation of epidermal growth factor receptor regulates fibronectin and transforming growth factor-beta synthesis via transcriptional and posttranscriptional mechanisms. Circ Res 1999;84:1073-84.[Abstract/Free Full Text]
- Ohkubo N., Matsubara H., NozawaY et al.Angiotensin type 2 receptors are reexpressed by cardiac fibroblasts from failing myopathic hamster hearts and inhibit cell growth and fibrillar collagen metabolism. Circulation 1997;96:3954-62.[Abstract/Free Full Text]
- Ichiki T., Kambayashi Y., Inagami T. Multiple growth factors modulate mRNA expression of angiotensin II type-2 receptor in R3T3 cells. Circ Res 1995;77:1070-6.[Abstract/Free Full Text]
- Nakamura S., Averill DB, Chappell MC, Diz DI, Brosnihan KB, Ferrario CM Angiotensin receptors contribute to blood pressure homeostasis in salt-depleted SHR. AmJPhysiol Regul Integr Comp Physiol 2003;284:R164-R173.
- Widdop RE, Gardiner SM, Kemp PA, Bennett T. Central administration of PD 123319 or EXP-3174 inhibits effects of angiotensin II. Am J Physiol 1993;264:H117-H125.[Web of Science][Medline]
[Order article via Infotrieve]
- Besse A., Trimoreau F., Praloran V., Denizot Y. Effect of cytokines and growth factors on the macrophage colony-stimulating factor secretion by human bone marrow stromal cells. Cytokine 2000;12:522-5.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Cao Y., Pearman AT, Zimmerman GA, McIntyre TM, Prescott SM Intracellular unesterified arachidonic acid signals apoptosis. ProcNatlAcadSci U S A 2000;97:11280-5.[CrossRef]
- Rizzo MT, Regazzi E., Garau D. et al. Induction of apoptosis by arachidonic acid in chronic myeloid leukemia cells. Cancer Res 1999;59:5047-53.[Abstract/Free Full Text]
Journal of Renin-Angiotensin-Aldosterone System, Vol. 5, No. 4,
176-182 (2004)
DOI: 10.3317/jraas.2004.037

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