Abstract
Bleeding and delayed healing of ulcers are well recognized clinical problems associated with the use of aspirin and other nonsteroidal antiinflammatory drugs, which have been attributed to their antiaggregatory effects on platelets. We hypothesized that antiplatelet drugs might interfere with gastric ulcer healing by suppressing the release of growth factors, such as vascular endothelial growth factor (VEGF), from platelets. Gastric ulcers were induced in rats by serosal application of acetic acid. Daily oral treatment with vehicle, aspirin, or ticlopidine (an ADP receptor antagonist) was started 3 days later and continued for 1 week. Ulcer induction resulted in a significant increase in serum levels of VEGF and a significant decrease in serum levels of endostatin (an antiangiogenic factor). Although both aspirin and ticlopidine markedly suppressed platelet aggregation, only ticlopidine impaired gastric ulcer healing and angiogenesis as well as reversing the ulcer-associated changes in serum levels of VEGF and endostatin. The effects of ticlopidine on ulcer healing and angiogenesis were mimicked by immunodepletion of circulating platelets, and ticlopidine did not influence ulcer healing when given to thrombocytopenic rats. Incubation of human umbilical vein endothelial cells with serum from ticlopidine-treated rats significantly reduced proliferation and increased apoptosis, effects reversed by an antibody directed against endostatin. Ticlopidine treatment resulted in increased platelet endostatin content and release. These results demonstrate a previously unrecognized contribution of platelets to the regulation of gastric ulcer healing. Such effects likely are mediated through the release from platelets of endostatin and possibly VEGF. As shown with ticlopidine, drugs that influence gastric ulcer healing may do so in part through altering the ability of platelets to release growth factors.
MeSH Terms
Angiogenesis Inhibitors/blood,physiology
Animals
Anti-Inflammatory Agents, Non-Steroidal/adverse effects,metabolism,therapeutic use
Apoptosis
Aspirin/adverse effects,metabolism,therapeutic use
Blood Platelets/drug effects,metabolism,physiology
Cell Division/drug effects
Cells, Cultured
Collagen/blood,physiology
Disease Models, Animal
Endostatins
Endothelial Growth Factors/blood,physiology
Endothelium, Vascular/cytology
Humans
Lymphokines/blood,physiology
Male
Neovascularization, Pathologic
Peptide Fragments/blood,physiology
Platelet Aggregation/drug effects
Platelet Aggregation Inhibitors/adverse effects,metabolism,therapeutic use
Rats
Rats, Wistar
Stomach Ulcer/blood,chemically induced,drug therapy,pathology
Ticlopidine/adverse effects,metabolism,therapeutic use
Vascular Endothelial Growth Factor A
Vascular Endothelial Growth Factors
Wound Healing/drug effects
Chemicals
Angiogenesis Inhibitors
Anti-Inflammatory Agents, Non-Steroidal
Endostatins
Endothelial Growth Factors
Lymphokines
Peptide Fragments
Platelet Aggregation Inhibitors
Vascular Endothelial Growth Factor A
Vascular Endothelial Growth Factors
Collagen
Ticlopidine
Aspirin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Ma L
Mucosal Inflammation Research Group, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, T2N 4N1, Canada.
Elliott S N
Cirino G
Buret A
Ignarro L J
Wallace J L
References (35)
35 references, click to expand
-
Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing.
Cancer Res. 1987 Feb 15;47(4):936-42
PMID: 3802100
-
Release of platelet-derived growth factor from human platelets by arachidonic acid.
Proc Natl Acad Sci U S A. 1979 Aug;76(8):4107-11
PMID: 291068
-
High-yield purification of platelet-derived endothelial cell growth factor: structural characterization and establishment of a specific antiserum.
Biochemistry. 1989 Feb 21;28(4):1704-10
PMID: 2541763
-
Tumor angiogenesis and metastasis--correlation in invasive breast carcinoma.
N Engl J Med. 1991 Jan 3;324(1):1-8
PMID: 1701519
-
Quality of gastric ulcer healing: a new, emerging concept.
J Clin Gastroenterol. 1991;13 Suppl 1:S42-7
PMID: 1719066
-
Thrombin structure and function: why thrombin is the primary target for antithrombotics.
Blood Coagul Fibrinolysis. 1991 Feb;2(1):69-75
PMID: 1772999
-
Release of different fractions of epidermal growth factor from human platelets in vitro: preferential release of 140 kDa fraction.
Regul Pept. 1992 Jan 23;37(2):95-100
PMID: 1531707
-
Thrombin promotes angiogenesis by a mechanism independent of fibrin formation.
Am J Physiol. 1993 May;264(5 Pt 1):C1302-7
PMID: 7684562
-
SR 25989 inhibits healing of a mechanical wound of confluent human saphenous vein endothelial cells which is modulated by standard heparin and growth factors.
J Cell Physiol. 1994 Aug;160(2):316-22
PMID: 7518823
-
A nitric oxide-releasing nonsteroidal anti-inflammatory drug accelerates gastric ulcer healing in rats.
Gastroenterology. 1995 Aug;109(2):524-30
PMID: 7615202
-
Anti-thrombotic effects of a nitric oxide-releasing, gastric-sparing aspirin derivative.
J Clin Invest. 1995 Dec;96(6):2711-8
PMID: 8675638
-
Protective effects of ticlopidine and aspirin, administered alone and in combination, on thrombus formation in rat cerebral vessels.
Haemostasis. 1996 May-Jun;26(3):150-6
PMID: 8738589
-
Endostatin: an endogenous inhibitor of angiogenesis and tumor growth.
Cell. 1997 Jan 24;88(2):277-85
PMID: 9008168
-
Nonsteroidal anti-inflammatory drugs and gastroenteropathy: the second hundred years.
Gastroenterology. 1997 Mar;112(3):1000-16
PMID: 9041264
-
Regulation of gastric epithelial cell growth by Helicobacter pylori: offdence for a major role of apoptosis.
Gastroenterology. 1997 Dec;113(6):1836-47
PMID: 9394723
-
Mechanisms of ulcer healing and effects of nonsteroidal anti-inflammatory drugs.
Am J Med. 1998 Mar 30;104(3A):43S-51S; discussion 79S-80S
PMID: 9572320
-
Coactivation of two different G protein-coupled receptors is essential for ADP-induced platelet aggregation.
Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8070-4
PMID: 9653141
-
Cyclooxygenase 1 contributes to inflammatory responses in rats and mice: implications for gastrointestinal toxicity.
Gastroenterology. 1998 Jul;115(1):101-9
PMID: 9649464
-
Peripheral blood platelets express VEGF-C and VEGF which are released during platelet activation.
Thromb Haemost. 1998 Jul;80(1):171-5
PMID: 9684805
-
In vitro release of vascular endothelial growth factor during platelet aggregation.
Am J Physiol. 1998 Sep;275(3 Pt 2):H1054-61
PMID: 9724313
-
Evidence that platelets promote tube formation by endothelial cells on matrigel.
Br J Pharmacol. 1998 Nov;125(6):1252-7
PMID: 9863654
-
Cigarette smoking delays ulcer healing: role of constitutive nitric oxide synthase in rat stomach.
Am J Physiol. 1999 Jan;276(1 Pt 1):G238-48
PMID: 9887001
-
Endostatin: yeast production, mutants, and antitumor effect in renal cell carcinoma.
Cancer Res. 1999 Jan 1;59(1):189-97
PMID: 9892206
-
Platelet: transporter of vascular endothelial growth factor.
Clin Cancer Res. 1997 Dec;3(12 Pt 1):2187-90
PMID: 9815613
-
In vivo antithrombotic effects of a nitric oxide-releasing aspirin derivative, NCX-4016.
Thromb Res. 1999 Jan 1;93(1):43-50
PMID: 10065898
-
The vascular endothelial growth factor family; proteins which guide the development of the vasculature.
Int J Exp Pathol. 1998 Oct;79(5):255-65
PMID: 10193309
-
Endostatin induces endothelial cell apoptosis.
J Biol Chem. 1999 Apr 23;274(17):11721-6
PMID: 10206987
-
Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding.
EMBO J. 1999 Aug 16;18(16):4414-23
PMID: 10449407
-
Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing.
Nat Med. 1999 Dec;5(12):1418-23
PMID: 10581086
-
Effects of clopidogrel on platelet activation and coagulation of non-anticoagulated rat blood under high shear stress.
Haemostasis. 1999;29(4):189-96
PMID: 10702699
-
The in vivo pharmacological profile of CS-747, a novel antiplatelet agent with platelet ADP receptor antagonist properties.
Br J Pharmacol. 2000 Apr;129(7):1439-46
PMID: 10742300
-
Growth factors in ulcer healing: lessons from recent studies.
J Physiol Paris. 2000 Mar-Apr;94(2):77-81
PMID: 10791686
-
A method for experimental, penetrating gastric and duodenal ulcers in rats. Observations on normal healing.
Am J Dig Dis. 1971 Mar;16(3):277-84
PMID: 5554507
-
Inhibition of platelet aggregation by a new agent, Ticlopidine.
Thromb Haemost. 1979 Feb 15;40(3):542-50
PMID: 425067
-
Adenosine diphosphate (ADP)-induced alpha-granules release from platelets of native whole blood is reduced by ticlopidine but not by aspirin or dipyridamole.
Thromb Haemost. 1986 Oct 21;56(2):147-50
PMID: 3810554