ATS
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Mohan R. Sarabu
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Rabbani, G.
Right arrow Articles by Gupte, S. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Rabbani, G.
Right arrow Articles by Gupte, S. A.
Related Collections
Right arrow Coronary disease
Right arrowRelated Article

Ann Thorac Surg 2007;83:510-515
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Regulation of Human Internal Mammary and Radial Artery Contraction by Extracellular and Intracellular Calcium Channels and Cyclic Adenosine 3', 5' Monophosphate

Golam Rabbani, MDa, Venkataramana Vijay, MDb, Mohan R. Sarabu, MDb, Sachin A. Gupte, MD, PhDa,*

a Department of Physiology, New York Medical College, Valhalla, New York
b Department of Cardiothoracic Surgery, New York Medical College, Valhalla, New York

Accepted for publication September 1, 2006.

* Address correspondence to Dr Gupte, Department of Physiology, Room 626, Basic Sciences Building, New York Medical College, Valhalla, NY 10595. (Email: sachin_gupte{at}nymc.edu).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: The internal mammary (IMA) and radial arteries (RA), which are routinely used in coronary artery bypass grafting, show a significant incidence of postoperative vasospasm. The present study evaluated the respective roles of calcium (Ca2+)–dependent and cyclic adenosine 3', 5' monophosphate–dependent (cAMP) signaling in mediating contraction and relaxation of the IMA and RA.

METHODS: We examined the contractile responses of the IMA and RA to potassium chloride, a depolarizing agent; phenylephrine, an {alpha}-adrenergic agonist; and U46619, a thromboxane analogue, in the absence and presence (0.045 to 1.500 mM) of extracellular Ca2+.

RESULTS: Potassium chloride elicited little or no contraction in the absence of extracellular Ca2+. Contractions elicited by U46619 were similar in the IMA and RA, both in the absence and presence of extracellular Ca2+. By contrast, phenylephrine elicited significantly greater extracellular Ca2+-dependent contraction of the IMA than the RA. Estimation of cyclic guanosine 3', 5' monophosphate (cGMP) and cAMP revealed levels of cAMP to be about fourfold higher than cGMP in both the RA and IMA. Whereas forskolin and milrinone elicited similar relaxation of IMA and RA precontracted with either U46619 or phenylephrine and increased adenylate cyclase-catalyzed cAMP production, isoproterenol-induced relaxation of the arteries precontracted with U46619 was significantly impaired compared with arteries precontracted with phenylephrine.

CONCLUSIONS: Our findings suggest that thromboxane A2 receptor–dependent pathways activate contraction of IMA and RA through both extracellular Ca2+-dependent and Ca2+-independent pathways. In addition, adenylate cyclase appears to play a key role in attenuating thromboxane A2 and {alpha}-adrenergic receptor-mediated contraction through both pathways.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The internal mammary (IMA) and radial arteries (RA), which are commonly used in coronary artery bypass grafting (CABG), are exposed to a variety of agents that promote vasoconstriction. During a CABG operation, for example, thromboxane A2 (TxA2) is released into the circulation upon injury to the endothelium or activation of platelets, and phenylephrine is routinely used as an inotropic support to maintain blood pressure [1]. Both of these agents have been implicated in postoperative vasospasm that can cause graft failure, although the mechanisms that underlie constriction of IMA and RA evoked by TxA2 and {alpha}-adrenergic agonists are poorly understood.

It is known that vascular smooth muscle contraction is elicited in part by induction of membrane depolarization and that the resultant influx of extracellular calcium (Ca2+) through L-type Ca2+ channels triggers Ca2+-induced Ca2+ release from intracellular stores [2, 3]. This in turn activates signaling pathways that lead to phosphorylation of myosin light chain kinase to sustain vasoconstriction. Moreover, it was recently shown that L-type Ca2+ channels mediate contraction of human IMA and RA stimulated by U46619, a stable TxA2 analogue, or the {alpha}-adrenergic agonists norepinephrine and phenylephrine [4].

The relative contributions of influx of extracellular Ca2+ and release of Ca2+ from intracellular stores to the contractile processes activated by U46619 and phenylephrine remain unknown. Therefore, one aim of the present study was to examine the mechanisms underlying contraction induced by membrane depolarization and also by TxA2-mediated and {alpha}-adrenergic-receptor–mediated signaling in the IMA and RA.

It is also well known that the endothelium-derived vasodilators stimulate relaxation induced by cyclic guanosine monophosphate (cGMP) and cyclic adenosine monophosphate (cAMP) and antagonize vasoconstriction. Both cGMP and cAMP induce relaxation of vascular smooth muscle by eliciting repolarization or hyperpolarization of the cell membrane and sequestration of Ca2+ in the sarcoplasmic reticulum [5, 6]. Notably, U46619 impairs endothelium-dependent and nitroglycerin-induced dilatation of RA by attenuating soluble guanylate cyclase–catalyzed cGMP production. On the other hand, cAMP-induced dilation of IMA and RA is unaffected by TxA2 receptor agonists [4].

Moreover, although papaverine and milrinone increase levels of cAMP in vascular smooth muscle and are used during CABG to dilate harvested vessels and prevent vasospasm, the role of cAMP in dilating the arterial grafts precontracted with TxA2 and {alpha}-adrenergic agonists remains unclear. Thus, a second objective of the current study was to investigate the capacity of cAMP to antagonize contraction of IMA and RA induced by TxA2-dependent and {alpha}-adrenergic-receptor–dependent signaling with the aim of better understanding the mechanisms of contraction/relaxation that lead to vasoconstriction or vasodilation of arterial grafts.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Drugs
Isoproterenol, forskolin, milrinone, and phenylephrine were all obtained from Sigma Chemical Company (St. Louis, MO). U46619 was from Cayman Chemical Company (Ann Arbor, MI). Other salts used in the study were from J. T. Baker Chemicals (Phillisburg, NJ).

Collection of Human Arteries
All experimental protocols were approved by our Institutional Review Board, and informed consent was obtained from all patients that participated in this study. Segments from distal sections of human IMA and RA surgical discards were collected from patients undergoing elective CABG surgery. The IMA and RA segments were immediately placed in ice-cold (4°C) plasmalyte solution and transported to the laboratory for tension studies.

Measurement of Isometric Tension
With the aid of a dissecting lens, IMA and RA segments were carefully cleaned of fat and connective tissue and cut into rings 3 to 4 mm in length. The endothelium was left intact. The arterial rings were mounted on wire hooks attached to force displacement transducers (Model FT-03, Grass Technologies, West Warwick, RI) for measurement of changes in isometric force, which were recorded on a polygraph (Model 7, Grass) as previously described [4, 7]. An optimal passive tension—the optimal point of contraction elicited by 30 mM KCl—for IMA (2 g) and RA (4 g) was determined from the length-tension relationships, after which the arteries were initially incubated for 2 hours at the optimal passive tension in individually thermostated (37°C) 10-mL baths (Metro Scientific, Farmingdale, NY) filled with Krebs bicarbonate buffer (pH 7.4; [in mM] 118 NaCl, 4.7 KCl, 1.5 CaCl2, 25 NaHCO3, 1.1 MgSO4, 1.2 KH2PO4, and 5.6 glucose) and gassed with 21% O2, 5% CO2, and 74% N2.

After the 2-hour equilibration, the vessels were depolarized with Krebs bicarbonate in which the NaCl was replaced with KCl, giving a final KCl concentration of 123 mM. This treatment enhanced the reproducibility of subsequent contractions. The arteries were then reequilibrated in normal Krebs solution for 20 to 30 minutes before the experiments were begun. In different sets of experiments, the effects of vasoconstrictors (phenylephrine and U46619) and vasodilators (isoproterenol, milrinone, and forskolin) were examined. Each individual ring was used for only one experiment with each of the agents studied.

Effects of Stimuli on Contraction
In this set of experiments, segments of IMA and RA were first contracted with KCl (123 mM) in Krebs solution. Then after washing out the KCl, subsequent contractile responses were expressed as percentages of the initial response to KCl. Segments of IMA and RA were placed in Ca2+-free Krebs solution containing ethylene glycol N', N', N', N' tetraacetic acid (0.1 mM) for 15 minutes, after which the contractile responses to KCl (30 mM), phenylephrine (10 µM), or U46619 (100 nM) were examined before and after by addition of CaCl2 (0.04 to 1.5 mM). Our aim here was to discriminate between contractile responses originating from the release of intracellular Ca2+ and those originating from the influx of extracellular Ca2+, as described elsewhere [8].

Estimation of cGMP and cAMP Levels and Adenylate Cyclase Activity
The levels of cGMP and cAMP in homogenates of IMA and RA were estimated after ether extraction by using a kit (Cayman Chemical Company). Briefly, tissue samples (50 mg) were homogenized in 500 µL of 50 mM phosphate buffer (pH 7.4) containing 15% trichloroacetic acid and then centrifuged at 15,000 rpm for 5 minutes at 4°C. The trichloroacetic acid was then removed from the supernatant by ether extraction, and the levels of the cyclic nucleotides present in the supernatant were estimated and expressed as per wet weight.

We determined adenylate cyclase activity using previously described protocols for estimating soluble guanylate cyclase activity with slight modification [9]. Briefly, each reaction mixture (0.2 mL final volume) contained 20 mM 3-(N-Morpholino) propanesulfonic acid (MOPS)-KOH (pH 7.4), 0.1 mM adenosine triphosphate (ATP), 2 mM MgCl2, 0.3 mM 3-isobutyl-1-methylxanthine (a phosphodiesterase inhibitor), an ATP-regenerating system consisting of 10 mM phosphocreatine and 150 U/mL creatine phosphokinase, 0.1 mL of homogenate, and the indicated test agents.

The assays were initiated by the addition of arterial protein. The reactions were run for 10 minutes at 37°C, after which they were terminated by addition of 0.1 mL of preheated 12 mM ethylene diamine tetraacetic acid. The assay mixtures were then boiled for 10 to 15 minutes, after which each tube was centrifuged at 15,000 rpm. The supernatant was then collected, diluted fivefold, and subjected to enzyme immunoassay to estimate cAMP. A 10-minute incubation for assay of adenylate cyclase activity was chosen to optimize the detection of cAMP under the wide variety of conditions tested. At the end of the incubation period, cAMP levels were determined after ether extraction using the enzyme immunoassay described above.

Statistical Analysis
Data are expressed as means ± standard error (SE). Arterial relaxation was measured as the percentage change in force from the precontracted steady-state level. The contractile force generated by the different contractile agents was expressed as the percentage change from the force generated by 123 mM KCl (IMA, 5.0 ± 0.3 g; and RA, 15.3 ± 1.5 g). The significance of differences among the results was analyzed using repeated measures analysis of variance post hoc Fisher’s least significant difference (protected t test) or Student’s t test.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
IMA and RA Contraction in the Absence of Extracellular Ca2+
Consistent with earlier findings [4], depolarization in 30 mM KCl induced 4.0 ± 0.3 g and 7.5 ± 1.7 g of force in IMA and RA, respectively, in the presence of normal extracellular Ca2+. By contrast, KCl had little or no effect on IMA (n = 10) or RA (n = 5) in the absence of extracellular Ca2+ (Figs 1A, 1B), indicating that KCl-induced contractions are entirely dependent on the influx of extracellular Ca2+. By contrast, U46619 and phenylephrine each elicited contraction of both arteries in the absence of extracellular Ca2+ (Figs 1A, 1B), although these contractions were significantly smaller than contractions elicited by U46619 (IMA, 96% ± 5%; RA, 130% ± 13%) and phenylephrine (IMA, 87% ± 6%; RA, 61% ± 7%) in the presence of normal extracellular Ca2+.


Figure 1
View larger version (24K):
[in this window]
[in a new window]

  		Fig 1. Contraction of the internal mammary artery (n = 10; A) and radial artery (n = 5; B) elicited in the absence of extracellular Ca2+ by potassium chloride (KCl; 30 mM; 30K, squares), phenylephrine (10 µM; Phen, down triangle) and U46619 (100 nM; U4, up triangle; C and D). After stabilization of contractions in the absence of extracellular Ca2+, addition of Ca2+ elicited concentration-dependent contraction of internal mammary artery (C) and radial artery (D). Range lines represent the standard error.

 
Contraction of IMA and RA in the Presence of Extracellular Ca2+
To further assess the dependence of IMA and RA contraction on extracellular Ca2+, we examined the effect of graded reintroduction of Ca2+ (0.045 to 1.500 mM) after stabilization of contractions in the absence of extracellular Ca2+. We found that a concentration of Ca2+ between 0.09 and 0.18 mM was required to initiate KCl-induced (30 mM) and U466190-induced (100 nM) contraction of IMA (Fig 1C) and RA (Fig 1D). In addition, although there was no significant difference in the amplitude of contractions elicited by either KCl or U46619 in IMA and RA (Figs 1C, 1D), phenylephrine-evoked contractions were significantly smaller in RA than IMA at all Ca2+ concentrations tested (Fig 1D).

Relaxation of IMA and RA Elicited by Isoproterenol, Milrinone, or Forskolin
To assess evoked relaxation, IMAs (n = 10) and RAs (n = 5) were precontracted to 70% of the 123 mM KCl-induced force using either phenylephrine (1 to 10 µM) or U46619 (10 to 50 nM). Once the contractions had stabilized, isoproterenol, which stimulates ß-adrenergic receptor-mediated cAMP production; milrinone, which inhibits cAMP-specific phosphodiesterase; and forskolin, which directly activates adenylate cyclase, all elicited arterial relaxation in a dose-dependent manner. However, isoproterenol elicited significantly greater (36% to 57%) relaxation of IMAs and RAs precontracted with phenylephrine than with U46619 (Figs 2A, 2B). Milrinone (Figs 2C, 2D) and forskolin (Figs 2E, 2F) relaxed both artery types to a similar degree, irrespective of whether they were precontracted with phenylephrine or U46619. However, a higher concentration (EC50) of forskolin (RA: 0.07 µM [U46619] versus 0.06 µM [phenylephrine] and IMA: 0.125 µM [U46619] versus 0.06 µM [phenylephrine]) and milrinone (RA: 20 µM [U46619] versus 0.06 µM [phenylephrine] and IMA: 1.10 µM [U46619] versus 0.45 µM [phenylephrine]) was required to evoke relaxation of RA and IMA precontracted with U46619 compared with arteries precontracted with phenylephrine.


Figure 2
View larger version (19K):
[in this window]
[in a new window]

  		Fig 2. Effects of a ß-adrenergic agonist, an adenylate cyclase activator, and a phosphodiesterase inhibitor on contraction of internal mammary artery (IMA; n = 10, circles) and radial artery (RA; n = 5, diamonds). Isoproterenol (A and B), milrinone (C and D), and forskolin (E and F) all dose-dependently relaxed IMA and RA precontracted with phenylephrine or U46619. Note that the lines representing the standard error are small and sometimes overlap the symbols.

 
Second Messenger Levels
Amongst the various mediators involved in regulating vasomotor activity, the second messengers, cGMP and cAMP, are widely recognized to play key roles in dilation processes. When we therefore estimated the cGMP and cAMP levels in IMA (n = 5; Fig. 3A) and RA (n = 5; Fig 3B), we found levels of cAMP to be significantly higher than those of cGMP in both the arteries.


Figure 3
View larger version (38K):
[in this window]
[in a new window]

  		Fig 3. Basal levels of cyclic guanosine 3', 5' monophosphate (cGMP) and cyclic adenosine 3', 5' monophosphate (cAMP) in unstimulated internal mammary artery (n = 5; A) and radial artery (n = 5; B). Range lines represent the standard error.

 
Adenylate Cyclase Activity
Finally, we compared adenylate cyclase activity in IMA (n = 5) and RA (n = 5; Fig 4) to assess the contribution made by evoked cAMP production to the relaxation of IMA and RA. Although basal adenylate cyclase activity was about fourfold higher in RA than IMA, direct activation of the enzyme by forskolin (10 µM) increased cAMP production by ninefold in IMA but by only twofold in RA. Adenylate cyclase activity also was significantly increased by isoproterenol (10 µM) and by milrinone (10 µM) in both artery types (Figs 4A, 4B). Notably, activation of adenylate cyclase by forskolin, isoproterenol, and milrinone was significantly diminished in the presence of U46619 (100 nM; Figs 4C, 4D). U46619 also reduced the basal enzyme activity to 50% to 60% of the control level in the two arteries.


Figure 4
View larger version (25K):
[in this window]
[in a new window]

  		Fig 4. Adenylate cyclase activity, estimated as a function of cyclic adenosine 3', 5' monophosphate (cAMP) levels, was increased in internal mammary artery (n = 5; A) and radial artery (n = 5; B) by forskolin (For), isoproterenol (Iso), and milrinone (Mil). Preconstriction of internal mammary artery (C) and radial artery (D) with U46619 significantly reduced activation of adenylate cyclase by forskolin, isoproterenol, and milrinone. Range lines represent the standard error.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
We have shown that both extracellular Ca2+-independent and Ca2+-dependent pathways mediate contraction of RA and IMA grafts evoked by depolarization-dependent and receptor-dependent mechanisms, and that activation of adenylate cyclase/cAMP-dependent signaling efficiently dilates IMA and RA precontracted with U44619, a stable TxA2 analogue, and phenylephrine, an {alpha}-adrenergic receptor agonist.

Segments of IMA and RA are routinely used in CABG for revascularization of the myocardium [10, 11]. Arterial grafts have an inherent propensity for vasospasm, however, which can lead to postoperative graft failure [12]. Several studies have shown TxA2 and {alpha}-adrenergic agonists to trigger such vasospasm [1, 13]; however, the mechanism(s) involved remain unclear. We therefore undertook this study in an effort to determine the role of Ca2+ in mediating contraction of RA and IMA evoked by U46619 and phenylephrine.

Although it was previously shown that stronger receptor-mediated contractions can be elicited in RA than IMA [14], and that RA grafts are more sensitive to TxA2 [1], our findings indicate that contractions elicited by U46619 did not significantly differ in the two artery types, either in the absence or presence of extracellular calcium (Fig 1). Given that U46619 induced significantly stronger contractions than did KCl, it seems reasonable to suggest that both influx of extracellular Ca2+ and release of Ca2+ from intracellular stores contribute to TxA2-induced vasospasm of arterial grafts.

TxA2 synthesis is stimulated by the inflammatory responses, platelet activation, angiotensin-II elevation, protamine-heparin complex, and hypoxia-reoxygenation during cardiopulmonary bypass surgery [15–18]. In addition, RA has a significantly higher basal thromboxane-to-prostacyclin ratio than IMA [4]. One might therefore expect that activation of TxA2 synthesis during CABG would trigger episodes of vasospasm more frequently in RA than in IMA. Interestingly, phenylephrine elicited only negligible contraction of these arteries in the absence of extracellular Ca2+, which suggests release of Ca2+ from intracellular stores does not play a predominant role in phenylephrine-induced contraction of RA and IMA. Our findings also indicate that phenylephrine elicits stronger contraction of IMA than RA, which is consistent with earlier reports [4, 13].

We therefore suggest that Ca2+-dependent contractile processes activated by {alpha}-adrenergic receptor agonists do not play a significant role in severely constricted RA grafts. Moreover, our findings collectively suggest that increases in intracellular Ca2+ resulting from both Ca2+ influx, presumably through voltage-gated and store-operated Ca2+ channels, and release of Ca2+ from the intracellular stores activated by TxA2 receptors and {alpha}-adrenergic receptors contribute to induction of severe constriction of IMA grafts.

Nitric oxide/cGMP-dependent relaxation of RA reportedly varies, depending on the eliciting stimulus [4, 19], whereas adenylate cyclase/cAMP-dependent relaxation of IMA is reportedly diminished by U46619 [20]. In addition, it is well established that vascular smooth muscle relaxation induced by ß-adrenergic receptor activation is dependent on cAMP signaling, which stimulates Ca2+ uptake by the sarcoplasmic reticulum, inhibits L-type Ca2+ channels, and reduces the Ca2+ sensitivity to the contractile apparatus [21]. Our data thus suggest that U46619 either impairs activation of adenylate cyclase or cAMP-dependent vasodilatory pathways, thereby reducing ß-adrenergic-receptor–mediated relaxation in IMA and RA. On the other hand, the fact that forskolin-evoked and milrinone-evoked relaxation of IMA and RA was unaffected by U44619 suggests cAMP-dependent signaling is not affected by the TxA2 analogue, despite its ability to reduce cAMP production by those two agents. Thus, in contrast to previous a study [22], our results demonstrate that U46619 inactivated adenylate cyclase and shifted the relaxation curve in IMA and RA.

In summary, we have shown that both influx of extracellular Ca2+ and release of Ca2+ from intracellular stores mediate contraction of IMA and RA elicited by TxA2, whereas {alpha}-adrenergic agonists elicit contraction mainly through activation of Ca2+ influx. We believe that the difference in the reactivity of RA and IMA to {alpha}-adrenergic agonists reflects, at least in part, a difference in the degree of Ca2+ influx. Our results also show that there are differences in the levels of basal cAMP in IMA and RA and that the IMA may have higher cAMP-dependent vasodilatory reserves than RA. Consequently, drugs activating the adenylate cyclase-cAMP axis could exert potentially beneficial effects that (1) moderate vasospasm induced by {alpha}-adrenergic agonists and TxA2, (2) prevent postoperative arterial graft failure, and (3) improve patency of the RA conduits in patients receiving RA grafts for myocardial revascularization.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported by AHA (grant # 0435070N).


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. He GW, Yang CQ, Starr A. Overview of the nature of vasoconstriction in arterial grafts for coronary operations Ann Thorac Surg 1995;59:676-683.[Abstract/Free Full Text]
  2. Gollasch M, Lohn M, Furstenau M, Nelson MT, Luft FC, Haller H. Ca2+ channels, Ca2+ sparks, and regulation of arterial smooth muscle function Z Kardiol 2000;89(Suppl 2):15-19.[Medline]
  3. Somlyo AP, Somlyo AV. Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase Physiol Rev 2003;83:1325-1358.[Abstract/Free Full Text]
  4. Arshad M, Vijay V, Floyd BC, et al. Thromboxane receptor stimulation suppresses guanylate cyclase-mediated relaxation of radial arteries Ann Thorac Surg 2006;81:2147-2154.[Abstract/Free Full Text]
  5. Takeuchi K, Watanabe H, Tran QK, et al. Nitric oxide: inhibitory effects on endothelial cell calcium signaling, prostaglandin I2 production and nitric oxide synthase expression Cardiovasc Res 2004;62:194-201.[Abstract/Free Full Text]
  6. Xiong Z, Sperelakis N. Regulation of L-type calcium channels of vascular smooth muscle cells J Mol Cell Cardiol 1995;27:75-91.[Medline]
  7. Gupte SA, Zias EA, Sarabu MS, Wolin MS. Role of prostaglandins in mediating differences in human internal mammary and radial artery relaxation elicited by hypoxia J Pharmacol Exp Ther 2004;311:510-518.[Abstract/Free Full Text]
  8. Iesaki T, Wolin MS. Thiol oxidation activates a novel redox-regulated coronary vasodilator mechanism involving inhibition of Ca2+ influx Arterioscler Thromb Vasc Biol 2000;20:2359-2365.[Abstract/Free Full Text]
  9. Gupte SA, Rupawalla T, Phillibert Jr D, Wolin MS. NADPH and heme redox modulate pulmonary artery relaxation and guanylate cyclase activation by NO Am J Physiol 1999;277:L1124-L1132.[Medline]
  10. Loop FD, Lytle BW, Cosgrove DM, et al. Influence of the internal-mammary-artery graft on 10-year survival and other cardiac events N Engl J Med 1986;314:1-6.[Abstract]
  11. Lytle BW, Blackstone EH, Loop FD, et al. Two internal thoracic artery grafts are better than one J Thorac Cardiovasc Surg 1999;117:855-872.[Abstract/Free Full Text]
  12. He GW. Arterial grafts for coronary artery bypass grafting: biological characteristics, functional classification, and clinical choice Ann Thorac Surg 1999;67:277-284.[Abstract/Free Full Text]
  13. Chardigny C, Jebara VA, Acar C, et al. Vasoreactivity of the radial arteryComparison with the internal mammary and gastroepiploic arteries with implications for coronary artery surgery. Circulation 1993;88:II115-II127.[Medline]
  14. He GW, Yang CQ. Radial artery has higher receptor-mediated contractility but similar endothelial function compared with mammary artery Ann Thorac Surg 1997;63:1346-1352.[Abstract/Free Full Text]
  15. Watkins WD, Peterson MB, Kong DL, et al. Thromboxane and prostacyclin changes during cardiopulmonary bypass with and without pulsatile flow J Thorac Cardiovasc Surg 1982;84:250-256.[Abstract]
  16. Stanke-Labesque F, Devillier P, Bedouch P, Cracowski JL, Chavanon O, Bessard G. Angiotensin II-induced contractions in human internal mammary artery: effects of cyclooxygenase and lipoxygenase inhibition Cardiovasc Res 2000;47:376-383.[Abstract/Free Full Text]
  17. Singh HP, Coleman ET, Hargrove M, Barrow SE, Murphy MB, Aherne T. Prostacyclin and thromboxane levels in pleural space fluid during cardiopulmonary bypass Ann Thorac Surg 1995;59:647-650.[Abstract/Free Full Text]
  18. Hobbhahn J, Conzen PF, Habazettl H, Gutmann R, Kellermann W, Peter K. Heparin reversal by protamine in humans—complement, prostaglandins, blood cells, and hemodynamics J Appl Physiol 1991;71:1415-1421.[Abstract/Free Full Text]
  19. Wei W, Yang CQ, Furnary A, He GW. Greater vasopressin-induced vasoconstriction and inferior effects of nitrovasodilators and milrinone in the radial artery than in the internal thoracic artery J Thorac Cardiovasc Surg 2005;129:33-40.[Abstract/Free Full Text]
  20. Cracowski JL, Stanke-Labesque F, Chavanon O, et al. Thromboxane A(2) modulates cyclic AMP relaxation and production in human internal mammary artery Eur J Pharmacol 2000;387:295-302.[Medline]
  21. Buhler FR, Bolli P, Erne P, et al. Adrenoceptors, calcium, and vasoconstriction in normal and hypertensive humans J Cardiovasc Pharmacol 1985;7(Suppl 6):S130-S136.
  22. He GW, Yang CQ. Characteristics of adrenoceptors in the human radial artery: clinical implications J Thorac Cardiovasc Surg 1998;115:1136-1141.[Abstract/Free Full Text]

Related Article

Invited commentary
Louis P. Perrault and Arnaud Mommerot
Ann. Thorac. Surg. 2007 83: 515-516. [Extract] [Full Text] [PDF]



This article has been cited by other articles:


Home page
 Ann. Thorac. Surg.Home page
L. P. Perrault and A. Mommerot
Invited commentary
Ann. Thorac. Surg., February 1, 2007; 83(2): 515 - 516.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Mohan R. Sarabu
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Rabbani, G.
Right arrow Articles by Gupte, S. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Rabbani, G.
Right arrow Articles by Gupte, S. A.
Related Collections
Right arrow Coronary disease
Right arrowRelated Article

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS