![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
CARDIOVASCULAR
-cyclodextrin Prevents Angiotensin II-Induced Tachyphylactic Contractile Responses in Rat AortaDepartment of Physiology (R.C.W., R.L.), Medical College of Georgia, Augusta, Georgia; and Department of Pharmacology and Toxicology (A.E.L., K.M.T., J.M.T., S.W.W.), Michigan State University, East Lansing, Michigan
Received March 26, 2007; accepted July 13, 2007.
 |
Abstract |
|---|
 Top Abstract Materials and MethodsResultsDiscussionReferences |
|---|
-cyclodextrin (CD), a drug that depletes cholesterol from the membrane and disassembles caveolae. CCEC-II to angiotensin II, but not to phenylephrine, was blunted in aortic rings treated with vehicle. In the presence of CD, CCEC-II did not differ significantly from CCEC-I for both agonists. CCEC-I to angiotensin II was abolished when in the presence of the AT1 receptor antagonist. The presence of AT1 receptors at the aortic smooth muscle cells' membrane treated with angiotensin II was observed by immunofluorescence only in the presence of CD. In addition, caveolin-1 coimmunoprecipitated with AT1 receptor after agonist stimulation, and this interaction was inhibited by CD. Our data suggest that caveolae are involved in the tachyphylactic contractile response induced by angiotensin II in rat aorta, and this effect is related to receptor internalization.
). Two distinct subtypes of angiotensin receptors, type I (AT1) and type II (AT2), have been identified, and both belong to the family of G protein-coupled receptors (de Gasparo et al., 2000). The biological actions in response to AT1 receptor activation are quite diverse, including contractile activity in vascular smooth muscle, aldosterone release from the adrenal gland, and growth-modulating effects on cardiac myocytes and smooth muscle cells (Timmermans et al., 1993). The biological actions of the AT2 receptor are less clear but seem to counterbalance the effects of the AT1 receptor (de Gasparo et al., 2000). The signal transduction pathways of the AT1 receptors, which mediate the major physiological effects of Ang II, are influenced by rapid internalization and desensitization of the receptor and long-term down-regulation of receptor expression (Thomas, 1999; Holloway et al., 2002). On the other hand, it has been shown that the AT2 receptor does not undergo internalization and desensitization (Hein et al., 1997).
The most accepted pathway for uptake of AT1 receptors is through accumulation in coated pits and rapid internalization via small coated vesicles (Bianchi et al., 1986; Anderson et al., 1993; Thomas, 1999; Gáborik et al., 2001). Although internalization via clathrin-coated vesicles is the major mechanism for G protein-coupled receptor endocytosis, certain receptors such as the bradykinin, endothelin-1, vasoactive intestinal peptide, muscarinic, and AT1 receptors have been reported to migrate to and/or be internalized through caveolae upon agonist stimulation and receptor activation (Feron et al., 1997; Haasemann et al., 1998; Ishizaka et al., 1998; Ushio-Fukai et al., 2001; Kule et al., 2004; Houndolo et al., 2005).
Caveolae are small invaginations at the plasma membrane enriched with cholesterol, glycosphingolipids, and the structural proteins caveolins that interact in vitro with a variety of signal-transducing molecules. Caveolin-1, a member of the protein caveolin family, is the major coat protein of caveolae (Anderson, 1998). Caveolae exist in most cell types and are particularly abundant in endothelial and smooth muscle cells (Ishizaka et al., 1998; Linder et al., 2005).
In rat aorta smooth muscle cells, AT1 receptors move to caveolin-enriched domains following angiotensin II stimulation (Ishizaka et al., 1998). Furthermore, plasma membrane cholesterol depletion inhibits angiotensin II-induced transactivation of the epidermal growth factor receptor (Ushio-Fukai et al., 2001), suggesting that caveolae/lipid rafts may function as a site of integration of events linking extracellular stimuli and intracellular effectors.
To maintain cardiovascular homeostasis and tight control of angiotensin II actions, cells have developed numerous mechanisms for regulating AT1 receptor activity and density, both acutely and chronically. For instance, angiotensin II stimulates potent vasoconstriction with an accompanying tachyphylaxis (De Mey and Vanhoutte, 1981; Sim and Kuttan, 1992), which is considered a protective device. The mechanism behind this tachyphylaxis is possibly due to internalization and desensitization of angiotensin II-mediated intracellular signaling.
In the present study, we hypothesized that AT1 receptor internalization by caveolae/lipid rafts mediates the tachyphylactic contractile response observed upon angiotensin II stimulation of rat aorta. The simplest approach to testing for tachyphylaxis in functional experiments is to determine whether the responses to an agonist are consistent upon repetition. Repeated contractile responses to angiotensin II were evaluated in rat aortic rings in the presence and absence of methyl--cyclodextrin, a drug that depletes plasma membrane cholesterol content, disrupting caveolae/lipid rafts (Ushio-Fukai et al., 2001), followed by immunohistochemistry experiments. Coimmunoprecipitation of caveolin-1 and AT1 receptor and electron microscopy to evaluate caveolar structures in aorta smooth muscle were also performed.
|
Materials and Methods |
|---|
|
TopAbstractMaterials and MethodsResultsDiscussionReferences |
|---|
In Vitro Measurement of Isometric Force Generation in Aortic Rings. After removal of fat and connective tissue, aortic rings (4 mm long) were mounted in an organ chamber for isometric tension recordings and bathed in physiological salt solution (PSS) of the following composition: 130.0 mM NaCl, 4.7 mM KCl, 1.2 mM KH2PO4, 1.2 mM MgSO4, 1.6 mM CaCl2, 14.9 mM NaHCO3, 0.03 mM EDTA, and 5.5 mM glucose, which was maintained at 37°C and bubbled with 95% O2 and 5% CO2. The endothelium was mechanically removed by gently rubbing the intimal surface with stainless steel wires. The aortic rings were set at 3.0g passive tension. Under this tension, optimal contractile responses were observed. After a 1-h equilibration period, vessels were contracted with phenylephrine (0.1 µM; Sigma-Aldrich, St. Louis, MO) and subsequently challenged with acetylcholine (10 µM; Sigma-Aldrich). The absence of relaxation to acetylcholine was considered as proof of endothelium denudation.
Increasing concentrations of angiotensin II (1 nM to 1 µM; Sigma-Aldrich) were added to the organ baths to obtain the first cumulative concentration-effect curve (CCEC-I) to this agonist. After the last concentration was added (1 µM) and the effect was obtained, the tissues were rinsed several times for 30 min until return to baseline. Methyl--cyclodextrin (10 mM; Sigma-Aldrich) was added for 60 min. After this period of incubation, a second cumulative concentration-effect curve (CCEC-II) to angiotensin II was constructed. Control responses were obtained in experiments where methyl--cyclodextrin was replaced by vehicle (PSS). All experiments were performed in the presence of indomethacin (1 µM; Sigma-Aldrich). At the end of CCEC-II, the aortic rings were embedded in optimal cutting transferase compound (Sakura Finetek USA, Inc., Torrance, CA) for immunohistochemistry procedures.
To evaluate the contribution of receptor activation to the contractile response elicited by angiotensin II, CCEC-I to angiotensin II was constructed in the presence of the angiotensin II receptor antagonist [Sar1 Leu8]angiotensin II (1 µM, 30 min; Sigma-Aldrich).
To evaluate desensitization during the CCEC, endothelium-denuded aortic rings were challenged with a single concentration of angiotensin II (1 or 10 µM), and the magnitude of contraction obtained with the concentrations given alone was compared with the magnitude of contraction induced by the same concentration in the CCEC.
To investigate whether the effects observed to angiotensin II were agonist-specific, CCEC-I and CCEC-II to phenylephrine (0.1 nM to 30 µM) were also constructed. For this purpose, CCEC-II to phenylephrine was constructed either in the presence of vehicle or methyl--cyclodextrin (10 mM), following the same experimental protocol for angiotensin II. Another set of experiments was performed in which CCEC-I to phenylephrine was replaced by angiotensin II (1 nM to 1 µM). CCEC-II to phenylephrine in the presence of vehicle after CCEC-I to angiotensin II was performed to evaluate the contribution of the downstream signaling pathways activated by angiotensin II in response to phenylephrine. The responses to phenylephrine were compared with the contractions induced by phenylephrine in similar experimental protocol with the exception that CCEC-I to angiotensin II was omitted.
Immunohistochemistry. Endothelium-denuded fresh-frozen sections (8-µm-thick) were thaw-mounted onto precleaned glass slides (Fisher Scientific Co., Pittsburgh, PA) and kept overnight in a desiccator at 4°C. After washing in phosphate-buffered saline (PBS) and fixation in acetone, slides were blocked with 10% normal goat serum (Jackson ImmunoResearch Laboratories, Inc., West Grove, PA) in PBS for 30 min at room temperature. The slices were then incubated with mouse monoclonal anti-caveolin-1 (final dilution 1:500; Research Diagnostics, Inc., Flanders, NJ) and rabbit polyclonal anti-AT1 antibodies (306 and N-10) (final dilution 1:200; Santa Cruz Biotechnology, Inc., Santa Cruz, CA). After washing in PBS, the fluorescent secondary antibodies, goat anti-mouse IgG Alexa Fluor 488, and goat anti-rabbit Alexa Fluor 594 (final dilution 1:1000; Invitrogen, Carlsbad, CA), were applied and incubated for 1 h at room temperature. Tissue autofluorescence was obtained in sections in which the primary antibodies were absent. After washing in PBS, the slides were coverslipped with anti-fading mounting medium (Gel/Mount medium; Biomeda Corp., Foster City, CA) and allowed to desiccate overnight at 4°C. Sections were viewed by confocal microscopy (Zeiss Confocal; Carl Zeiss Inc., Thornwood, NY).
Immunoprecipitation. Endothelium-denuded aortic rings were divided in four different groups receiving vehicle (PSS) or methyl--cyclodextrin (10 mM) for 40 min at 37°C. After the incubation time, vehicle or angiotensin II (1 µM) was administered for 20 min before being snap-frozen (vehicle + vehicle; vehicle + angiotensin II; methyl--cyclodextrin + vehicle; methyl--cyclodextrin + angiotensin II). The tissues were pulverized in liquid nitrogen and solubilized with lysis buffer (125 M Tris HCl, pH 6.8, 4% sodium dodecyl sulfate, and 20% glycerol), with protease inhibitors (0.5 mM phenylmethylsulfonyl fluoride, 10 µg/ml aprotinin, and 10 µg/ml leupeptin) and the phosphatase inhibitor sodium orthovanadate (1 mM). Homogenates were centrifuged (11,000g for 10 min, 4°C), and supernatant total protein was measured. Samples (500-µg protein) were divided, and immunoprecipitation was performed using Protein A/G Plus-Agarose (30 µl; Santa Cruz Biotechnology), with or without anti-caveolin-1 antibody (3.75 µg/sample overnight; Fitzgerald Industries International Inc., Concord, MA; or clone Z034, 5 µg/sample overnight; Zymed Laboratories, South San Francisco, CA). After extensive washing, samples were separated by 15% SDS-polyacrylamide gel electrophoresis and transferred to polyvinylidene difluoride membranes. Membranes were blocked with PBS containing nonfat dry milk (5%) and bovine serum albumin (2%), probed overnight with antibody against AT1 receptor (N-10, 1:200; Santa Cruz Biotechnology) or against caveolin-1 (1:1000; Fitzgerald Industries International Inc., or Zymed Laboratories), washed, and incubated with horseradish peroxidase-conjugated goat anti-rabbit (1:1000, 1 h; Cell Signaling Technology Inc., Danvers, MA) or anti-mouse (1:1000, 1 h; GE Healthcare, Little Chalfont, Buckinghamshire, UK) antibodies, respectively. The ECL Western blotting system was used for detection. In some experiments, lysates were subjected to immunoblotting without immunoprecipitation.
Electron Microscopy. Aortic segments treated with methyl--cyclodextrin (10 mM) or vehicle (PSS) for 1 h were fixed overnight at 4°C in a solution consisting of 2% glutaraldehyde, 2% paraformaldehyde dissolved in sodium cacodylate buffer (0.1 M) containing sucrose. Samples were washed with sodium cacodylate buffer (0.1 M) and then postfixed in 4% osmium tetroxide for 1 h. Samples were dehydrated through a graded series of alcohol and embedded in Epon 812 resin with Araldite (Electron Microscopy Sciences, Hatfield, PA). Ultra-thin sections were double-stained with alcoholic uranyl acetate and lead citrate and examined with a JEOL-1010 transmission electron microscope (JEOL, Tokyo, Japan).
Data Analysis. Sensitivity to an agonist was expressed as pD2 = –log EC50 calculated by nonlinear regression. Data were analyzed by Student's t test for paired or unpaired comparisons. Additional statistical analyses were performed using one-way analysis of variance followed by the Student-Newman-Keuls post hoc test for multiple comparisons. A value of P < 0.05 was considered statistically significant. Isometric force generation data were measured as contraction in milligrams and expressed as mean ± S.E.M.
|
Results |
|---|
|
TopAbstractMaterials and MethodsResultsDiscussionReferences |
|---|
|
-Cyclodextrin Prevents the Tachyphylactic Contractile Responses to Angiotensin II. In the presence of methyl--cyclodextrin, the contraction induced by angiotensin II in rat aortic rings in CCEC-II (pD2 = 8.2 ± 0.01; maximal effect = 813 ± 172, n = 10) was similar to that observed in the CCEC-I (pD2 = 7.7 ± 0.1; maximal effect = 981 ± 183, n = 10; P > 0.05) (Fig. 2).
|
Phenylephrine Does Not Induce Tachyphylactic Contractile Responses. After incubation with vehicle, CCEC-II to phenylephrine (pD2 = 8.2 ± 0.3; maximal response = 1771 ± 360 mg) was similar to CCEC-I to phenylephrine (8.4 ± 0.2; maximal response = 1861 ± 297 mg, n = 5, P > 0.05) (Fig. 3A). Another set of experiments was performed in which CCEC-I to phenylephrine was replaced by angiotensin II (1 nM to 1 µM). Previous stimulation with angiotensin II had no effect on phenylephrine-induced contraction compared with the contractions to phenylephrine obtained in similar experiments in which angiotensin II was omitted (P > 0.05, n = 6; data not shown).
|
-Cyclodextrin Has No Effect on Phenylephrine-Induced Contractile Responses. In the presence of methyl--cyclodextrin, CCEC-II to phenylephrine (pD2 = 8.1 ± 0.2, maximal response = 1551 ± 154 mg) was not different from CCEC-I (pD2 = 8.1 ± 0.1; maximal response = 1729 ± 154 mg, n = 5, P > 0.05) (Fig. 3B).
Methyl--Cyclodextrin Disassembles Smooth Muscle Caveolae. The effect of methyl--cyclodextrin (10 mM) on the structure of aortic smooth muscle membrane was evaluated by transmission electron microscopy. Micrographs of smooth muscle cell membrane in control vessels show the presence of caveolae at the plasma membrane that are mostly disassembled in samples treated with methyl--cyclodextrin (Fig. 4).
|
Methyl--Cyclodextrin Prevents AT1 Receptor Internalization. Caveolin-1 and AT1 receptor localization is shown by confocal immunofluorescence microscopy in endothelium-denuded aortic sections (Fig. 5A). AT1 receptor [antibody anti-AT1 (N-10)] was visualized using a red fluorescent secondary antibody, whereas caveolin-1 was visualized with a green fluorescent secondary antibody. A wide distribution of AT1 receptor and caveolin-1 was observed only in aortic vessels treated with methyl--cyclodextrin. The overlay of pseudocolored red and green images, resulting in a yellow signal at sites of colocalization can also be observed. In the aortic sections treated with vehicle, a lack of signal for AT1 receptors was observed. Similar results were obtained when the antibody anti-AT1 (306) was used (data not shown). The signal obtained by incubation with the red (Alexa Fluor 594) and green (Alexa Fluor 488) secondary antibodies alone representing tissue autofluorescence is shown in Fig. 5B.
|
-Cyclodextrin. Figure 6 shows that coimmunoprecipitation of AT1 receptor and caveolin-1 (control) was increased after stimulation with Ang II. Methyl--cyclodextrin had no effect when given alone, whereas it inhibited coimmunoprecipitation of AT1 and caveolin-1 after stimulation with angiotensin II. The anti-caveolin-1 antibody recognized a protein band of 22 kDa in homogenates precipitated with the same antibody, and the anti-AT1 receptor antibody recognized a protein of 43 kDa in nonprecipitated aorta samples (data not shown).
|
|
Discussion |
|---|
|
TopAbstractMaterials and MethodsResultsDiscussionReferences |
|---|
Angiotensin II and Tachyphylaxis. Most of the actions of angiotensin II have been attributed to stimulation of the AT1 receptor whose effects are frequently subject to tachyphylaxis or desensitization. Indeed, we observed failure of angiotensin II to induce reproducible contractions after repeated stimulation (Fig. 1), a phenomenon known as tachyphylaxis.
The findings reported in the present study were obtained in endothelium-denuded rat aortic rings to avoid the mediation of endothelial factors. Unpublished data from our laboratory show tachyphylactic contractile response to angiotensin II in endothelium-intact aortic rings. However, the presence of the endothelium caused a significant decrease in angiotensin II-induced contraction. Augmented contractile responses to angiotensin II after removal of the endothelium has also been reported by others in aortic tissues (Gruetter et al., 1988; Hardy et al., 2001). To avoid the contribution and/or interference of endothelium-derived factors to the contraction induced by angiotensin II and thereby to tachyphylaxis, the results obtained in endothelium intact aortic rings were not included in the present work.
The underlying mechanisms accounting for receptor desensitization or tachyphylaxis may include uncoupling of the receptor-transduction system, molecular interaction with the receptor, receptor down-regulation, and receptor internalization (Thomas, 1999; Hunyady et al., 2000; Holloway et al., 2002; Motta et al., 2003).
Desensitization to angiotensin II during the concentration-effect curve does not contribute to the tachyphylactic contractile responses, as evidenced by the lack of differences between the magnitude of contraction obtained by a given concentration of angiotensin II alone or in the concentration-effect curve. Moreover, the fact that phenylephrine-induced contraction was not affected by previous exposure to angiotensin II indicates that desensitization of the signal transduction pathway mediating angiotensin II responses is not the cause for the inability of angiotensin II to induce reproducible contractions.
The phenomenon of tachyphylaxis is not peculiar to angiotensin II, because tachyphylactic responses have also been reported for other agonists, such as endothelin-1 (Linder and Bendhack, 2002) and serotonin (De Mey and Vanhoutte, 1981). However, phenylephrine-induced contraction in rat aorta was not tachyphylactic, as shown in the present study (Fig. 3A) and in previous studies by others (Robertson et al., 1994). These data suggest that the tachyphylactic responses to angiotensin II in rat aorta is specifically linked to AT1 receptor.
Angiotensin II and Caveolae. In this study, we observed that methyl--cyclodextrin prevents angiotensin II-induced tachyphylactic responses (Fig. 2), whereas it had no effect in phenylephrine-induced contraction (Fig. 3B). The cholesterol-binding agent, methyl--cyclodextrin, has been used as a pharmacological tool to study the role of caveolae/lipid rafts in vascular reactivity (Kaiser et al., 2002; Je et al., 2004). We observed disruption of caveolae in aorta treated with methyl--cyclodextrin (Fig. 4).
One of the limitations of the present study is the use of methyl--cyclodextrin as the sole technique to disrupt caveolae. In addition to cyclodextrin, filipin is another cholesterol-binding agent used as a pharmacological tool to study the role of caveolae. Filipin, known to sequester cholesterol, modifies cholesterol interactions with other plasmalemmal components and, consequently, the organization and properties of the caveolae, and it subsequently causes the caveolae components to disassemble (McGookey et al., 1983). However, in the unpublished data from our laboratory, we observed that filipin causes contraction of rat aortic rings, excluding this compound as an alternative technique to study caveolae.
Supporting the use of methyl--cyclodextrin to disrupt caveolae, unpublished data from our laboratory showed reconstitution of disassembled caveolae after the addition of cholesterol back to cholesterol-depleted aortic tissues. In addition, in aortic vascular smooth muscle cells, methyl--cyclodextrin disassembles caveolae in association with membrane cholesterol depletion (Ishizaka et al., 1998).
We also observed increased interaction of the caveolar protein marker, caveolin-1, and AT1 receptor following angiotensin II stimulation (Fig. 6). Similar results were reported by Ishizaka et al. (1998) in rat aortic cells. Moreover, methyl--cyclodextrin inhibits the interaction between AT1 and caveolin-1 (Fig. 6). Later investigations have demonstrated the importance of caveolae/lipid rafts for angiotensin II-induced intracellular signaling (Ushio-Fukai et al., 2001; Zuo et al., 2005). These data suggest that caveolae/lipid rafts are therefore regulatory platforms for the cascade of events resulting in angiotensin II responses.
Angiotensin II, Receptor Internalization, and Caveolae. Like other G protein-coupled receptors, AT1 receptors undergo a process of agonist-induced receptor-mediated endocytosis or internalization (Hein et al., 1997; Hunyady et al., 2000; Gáborik et al., 2001; Holloway et al., 2002; Zhuo et al., 2002; Wyse et al., 2003; Kule et al., 2004). Clathrin-coated pits are the most common pathway for angiotensin II receptor internalization (Bianchi et al., 1986; Thomas, 1999; Gáborik et al., 2001; Fessart et al., 2005). However, whereas Gáborik et al. (2001) observed that inducing caveolae components to disassemble had no effect on angiotensin II receptor internalization, Kule et al. (2004) reported that a fraction of AT1A receptor internalization is mediated by caveolae. A growing body of evidence has emerged showing receptor internalization via clathrin-independent pathways. Furthermore, progress has been made in characterizing a pathway involving the caveolae/lipid rafts domains in receptor internalization (Ishizaka et al., 1998; Bari et al., 2005; Houndolo et al., 2005).
Interestingly, we observed AT1 membrane localization in experimental conditions in which the tachyphylactic responses to angiotensin II were prevented by methyl--cyclodextrin (Fig. 5A), whereas no receptor localization at the plasma membrane was observed in the condition where tachyphylaxis was observed. These data suggest that caveolae disruption prevents AT1 receptor internalization and thus support the continued response to angiotensin II.
There is evidence that internalization of the AT1 receptor is not the most important mechanism involved in the manifestation of angiotensin II-induced contraction and desensitization/tachyphylaxis in smooth muscle as reported by Kanashiro et al. (1995). These authors present evidence that tachyphylaxis to angiotensin II in the guinea pig ileum is most probably due to conformational change of the angiotensin II receptor complex within the plasma membrane. Also confronting our findings is the work by Wyse et al. (2003). These authors show that AT1 receptor migrates to noncaveolar lipid rafts domains following angiotensin II stimulation. Furthermore, the authors observed interaction between caveolin-3 and AT1 receptor in the Golgi and endoplasmic reticulum, suggesting that caveolins are rather involved in the exocytic pathway than in receptor internalization. In the unpublished data from our laboratory, we observed that phenylarsine oxide, a compound widely used to inhibit receptor internalization (Griendling et al., 1986; Lázari et al., 1997; Goggi et al., 2007), abolished the contraction induced by angiotensin II. However, it also abolished the contraction induced by membrane depolarization in addition to the contraction mediated by receptor activation. These data exclude the use of this compound as an alternative choice to study the effect of receptor internalization in contraction. Thus, whether receptor internalization is the main cause for tachyphylaxis requires further investigation.
All together, the unique finding of the present study reveals caveolae as mediators in the tachyphylactic contraction induced by angiotensin II in rat aorta. Tachyphylaxis is probably a protective action taken by cells to prevent exacerbation of the effects of the renin-angiotensin system and may be impaired in aging and hypertension. Understanding the mechanisms involved in caveolae mediating the tachyphylactic responses to angiotensin II following AT1 receptor activation may represent a new avenue for the treatment of cardiovascular diseases associated with hyperactivity of the renin-angiotensin system.
|
Footnotes |
|---|
Article, publication date, and citation information can be found at http://jpet.aspetjournals.org.
ABBREVIATIONS: AT1, angiotensin II type I; AT2, angiotensin II type II; Ang II, angiotensin II; CD, methyl--cyclodextrin; CCEC-I, first cumulative concentration-effect curve; CCEC-II, second cumulative concentration-effect curve; PSS, physiological salt solution; PBS, phosphate-buffered saline.
Address correspondence to: Dr. A. Elizabeth Linder, Michigan State University, Department of Pharmacology and Toxicology, B-445 Life Sciences Building, East Lansing, MI 48824-1317. E-mail: linderau{at}msu.edu
|
References |
|---|
|
TopAbstractMaterials and MethodsResultsDiscussionReferences |
|---|
Anderson KM, Murahashi T, Dostal DE, and Peach MJ (1993) Morphological and biochemical analysis of angiotensin II internalization in cultured rat aortic smooth muscle cells. Am J Physiol 264: C179–C188.[Medline]
Anderson RG (1998) The caveolae membrane system. Annu Rev Biochem 67: 199–225.[CrossRef][Medline]
Bari M, Battista N, Fezza F, Finazzi-Agro A, and Maccarrone M (2005) Lipid rafts control signaling of type-1 cannabinoid receptors in neuronal cells. Implications for anandamide-induced apoptosis. J Biol Chem 280: 12212–12220.
Bianchi C, Gutkowska J, Charbonneau C, Ballak M, Anand-Srivastava MB, De Lean A, Genest J, and Cantin M (1986) Internalization and lysosomal association of [125I]angiotensin II in norepinephrine-containing cells of the rat adrenal medulla. Endocrinology 119: 1873–1875.
de Gasparo M, Catt KJ, Inagami T, Wright JW, and Unger T (2000) International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 52: 415–472.
De Mey C and Vanhoutte PM (1981) Effect of age and spontaneous hypertension on the tachyphylaxis to 5-hydroxytryptamine and angiotensin II in the isolated rat kidney. Hypertension 3: 718–724.
Feron O, Smith TW, Michel T, and Kelly RA (1997) Dynamic targeting of the agonist-stimulated m2 muscarinic acetylcholine receptor to caveolae in cardiac myocytes. J Biol Chem 272: 17744–17748.
Fessart D, Simaan M, and Laporte SA (2005) c-Src regulates clathrin adapter protein 2 interaction with beta-arrestin and the angiotensin II type 1 receptor during clathrin-mediated internalization. Mol Endocrinol 19: 491–503.
Gáborik Z, Szaszak M, Szidonya L, Balla B, Paku S, Catt KJ, Clark AJ, and Hunyady L (2001) -Arrestin- and dynamin-dependent endocytosis of the AT1 angiotensin receptor. Mol Pharmacol 59: 239–247.
Goggi JL, Sardini A, Egerton A, Strange PG, and Grasby PM (2007) Agonist-dependent internalization of D2 receptors: imaging quantification by confocal microscopy. Synapse 61: 231–241.[CrossRef][Medline]
Griendling KK, Rittenhouse SE, Brock TA, Ekstein LS, Gimbrone MA Jr, and Alexander RW (1986) Sustained diacylglycerol formation from inositol phospholipids in angiotensin II-stimulated vascular smooth muscle cells. J Biol Chem 261: 5901–5906.
Gruetter CA, Ryan ET, Lemke SM, Bailly DA, Fox MK, and Schoepp DD (1988) Endothelium-dependent modulation of angiotensin II-induced contraction in blood vessels. Eur J Pharmacol 146: 85–95.[CrossRef][Medline]
Haasemann M, Cartaud J, Muller-Esterl W, and Dunia I (1998) Agonist-induced redistribution of bradykinin B2 receptor in caveolae. J Cell Sci 111: 917–928.[Abstract]
Hardy G, Stanke-Labesque F, Peoc'h M, Hakim A, Devillier P, Caron F, Morel S, Faure P, Halimi S, and Bessard G (2001) Cysteinyl leukotrienes modulate angiotensin II constrictor effects on aortas from streptozotocin-induced diabetic rats. Arterioscler Thromb Vasc Biol 21: 1751–1758.
Hein L, Meinel L, Pratt RE, Dzau VJ, and Kobilka BK (1997) Intracellular trafficking of angiotensin II and its AT1 and AT2 receptors: evidence for selective sorting of receptor and ligand. Mol Endocrinol 11: 1266–1277.
Holloway AC, Qian H, Pipolo L, Ziogas J, Miura S, Karnik S, Southwell BR, Lew MJ, and Thomas WG (2002) Side-chain substitutions within angiotensin II reveal different requirements for signaling, internalization, and phosphorylation of type 1A angiotensin receptors. Mol Pharmacol 61: 768–777.
Houndolo T, Boulay PL, and Claing A (2005) G protein-coupled receptor endocytosis in ADP-ribosylation factor 6-depleted cells. J Biol Chem 280: 5598–5604.
Hunyady L, Catt KJ, Clark AJ, and Gaborik Z (2000) Mechanisms and functions of AT1 angiotensin receptor internalization. Regul Pept 91: 29–44.[CrossRef][Medline]
Ishizaka N, Griendling KK, Lassegue B, and Alexander RW (1998) Angiotensin II type 1 receptor: relationship with caveolae and caveolin after initial agonist stimulation. Hypertension 32: 459–466.
Je HD, Gallant C, Leavis PC, and Morgan KG (2004) Caveolin-1 regulates contractility in differentiated vascular smooth muscle. Am J Physiol Heart Circ Physiol 286: H91–H98.
Kaiser RA, Oxhorn BC, Andrews G, and Buxton IL (2002) Functional compartmentation of endothelial P2Y receptor signaling. Circ Res 91: 292–299.
Kanashiro CA, Paiva TB, Paiva AC, Prioste RN, Aboulafia J, and Shimuta SI (1995) Angiotensin II tachyphylaxis in the guinea pig ileum and its prevention: a pharmacological and biochemical study. J Pharmacol Exp Ther 275: 1543–1550.
Kule CE, Karoor V, Day JN, Thomas WG, Baker KM, Dinh D, Acker KA, and Booz GW (2004) Agonist-dependent internalization of the angiotensin II type one receptor (AT1): role of C-terminus phosphorylation in recruitment of beta-arrestins. Regul Pept 120: 141–148.[CrossRef][Medline]
Lázari MF, Porto CS, Freymuller E, Abreu LC, and Picarelli ZP (1997) Receptor-mediated endocytosis of angiotensin II in rat myometrial cells. Biochem Pharmacol 54: 399–408.[CrossRef][Medline]
Linder AE and Bendhack LM (2002) Endothelin-1-induced contraction is impaired in the tail artery of renal hypertensive rats. Vasc Pharmacol 39: 77–82.[CrossRef]
Linder AE, McCluskey LP, Cole KR 3rd, Lanning KM, and Webb RC (2005) Dynamic association of nitric oxide downstream signaling molecules with endothelial caveolin-1 in rat aorta. J Pharmacol Exp Ther 314: 9–15.
McGookey DJ, Fagerberg K, and Anderson RG (1983) Filipin-cholesterol complexes form in uncoated vesicle membrane derived from coated vesicles during receptor-mediated endocytosis of low density lipoprotein. J Cell Biol 96: 1273–1278.
Motta SC, Poletti EF, Souza SE, Correa SA, Jubilut GN, Paiva AC, Shimuta SI, and Nakaie CR (2003) Tachyphylactic properties of angiotensin II analogs with bulky and hydrophobic substituents at the N-terminus. J Pept Res 62: 227–232.[CrossRef][Medline]
Robertson MJ, Wragg A, and Clark KL (1994) Modulation of tachyphylaxis to angiotensin II in rabbit isolated aorta by the angiotensin AT1 receptor antagonist, losartan. Regul Pept 50: 137–145.[CrossRef][Medline]
Sim MK and Kuttan SC (1992) Effects of noradrenaline and prostaglandin F2 alpha on angiotensin-induced contraction and tachyphylaxis in rat aortic rings. Pharmacol Toxicol 70: 60–64.[Medline]
Thomas WG (1999) Regulation of angiotensin II type 1 (AT1) receptor function. Regul Pept 79: 9–23.[CrossRef][Medline]
Timmermans PB, Wong PC, Chiu AT, Herblin WF, Benfield P, Carini DJ, Lee RJ, Wexler RR, Saye JA, and Smith RD (1993) Angiotensin II receptors and angiotensin II receptor antagonists. Pharmacol Rev 45: 205–251.[Medline]
Ushio-Fukai M, Hilenski L, Santanam N, Becker PL, Ma Y, Griendling KK, and Alexander RW (2001) Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells: role of cholesterol-rich microdomains and focal adhesions in angiotensin II signaling. J Biol Chem 276: 48269–48275.
Wyse BD, Prior IA, Qian H, Morrow IC, Nixon S, Muncke C, Kurzchalia TV, Thomas WG, Parton RG, and Hancock JF (2003) Caveolin interacts with the angiotensin II type 1 receptor during exocytic transport but not at the plasma membrane. J Biol Chem 278: 23738–23746.
Zhuo JL, Imig JD, Hammond TG, Orengo S, Benes E, and Navar LG (2002) Ang II accumulation in rat renal endosomes during Ang II-induced hypertension: role of AT(1) receptor. Hypertension 39: 116–121.
Zuo L, Ushio-Fukai M, Ikeda S, Hilenski L, Patrushev N, and Alexander RW (2005) Caveolin-1 is essential for activation of Rac1 and NAD(P)H oxidase after angiotensin II type 1 receptor stimulation in vascular smooth muscle cells: role in redox signaling and vascular hypertrophy. Arterioscler Thromb Vasc Biol 25: 1824–1830.
This article has been cited by other articles:
|
|
 |
|
  Z. Bagi, N. Erdei, and A. Koller High intraluminal pressure via H2O2 upregulates arteriolar constrictions to angiotensin II by increasing the functional availability of AT1 receptors Am J Physiol Heart Circ Physiol, August 1, 2008; 295(2): H835 - H841. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
 |
 |
 |
|
 |
 |
 |
