Original Article

Nitric Oxide as a Mediator of Relaxation of the Corpus Cavernosum in Response to Nonadrenergic, Noncholinergic Neurotransmission

Jacob Rajfer, M.D., William J. Aronson, M.D., Peggy A. Bush, B.S., Frederick J. Dorey, Ph.D., and Louis J. Ignarro, Ph.D.

N Engl J Med 1992; 326:90-94January 9, 1992

Abstract

Abstract

Background.

Nitric oxide has been identified as an endothelium-derived relaxing factor in blood vessels. We tried to determine whether it is involved in the relaxation of the corpus cavernosum that allows penile erection. The relaxation of this smooth muscle is known to occur in response to stimulation by nonadrenergic, noncholinergic neurons.

Full Text of Background. ...

Methods.

We studied strips of corpus cavernosum tissue obtained from 21 men in whom penile prostheses were inserted because of impotence. The mounted smooth-muscle specimens were pretreated with guanethidine and atropine and submaximally contracted with phenylephrine. We then studied the smooth-muscle relaxant responses to stimulation by an electrical field and to nitric oxide.

Full Text of Methods. ...

Results.

Electrical-field stimulation caused a marked, transient, frequency-dependent relaxation of the corpus cavernosum that was inhibited in the presence of N-nitro-L-arginine and N-amino-L-arginine, which selectively inhibit the biosynthesis of nitric oxide from L-arginine. The addition of excess L-arginine, but not D-arginine, largely reversed these inhibitory effects. The specific liberation of nitric oxide (by S-nitroso-N-acetylpenicillamine) caused rapid, complete, and concentration-dependent relaxation of the corpus cavernosum. The relaxation caused by either electrical stimulation or nitric oxide was enhanced by a selective inhibitor of cyclic guanosine monophosphate (GMP) phosphodiesterase (M&B 22,948). Relaxation was inhibited by methylene blue, which inhibits cyclic GMP synthesis.

Full Text of Results. ...

Conclusions.

Our findings support the hypothesis that nitric oxide is involved in the nonadrenergic, noncholinergic neurotransmission that leads to the smooth-muscle relaxation in the corpus cavernosum that permits penile erection. Defects in this pathway may cause some forms of impotence. (N Engl J Med 1992;326:90–4.)

Full Text of Conclusions. ...

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Article

IMPOTENCE is a major clinical problem of adult men. In the United States alone, approximately 10 million men suffer from dysfunction of penile erection. Annually, erectile dysfunction results in more than 400,000 outpatient visits and 30,000 hospital admissions.1 2 3 In the majority of patients, abnormal vascular responsiveness is the underlying cause of impotence, and failure to retain blood within the sinusoids is the most common cause of vasculogenic impotence.4 , 5 Filling of the sinusoidal spaces compresses the outflow venules against the relatively rigid tunica albuginea, causing engorgement of the corpus cavernosum with blood.6 , 7 Thus, failure of penile erection could be due to impaired relaxation of the smooth muscle of the corpus cavernosum.

It has been shown that corporal smooth muscle relaxes markedly in response to stimulation by nonadrenergic, noncholinergic neurons8 , 9 and that relaxation elicited by acetylcholine is mediated by a chemical substance derived from the endothelium.8 The endothelium may not play an obligatory part in the relaxation of the corpus cavernosum elicited by nonadrenergic, noncholinergic neurons,10 but this has not been firmly established. Several endogenous peptides, such as vasoactive intestinal peptide and substance P, have been proposed as causes of the relaxation of corpus cavernosum.11 12 13 14 We previously reported that relaxation of rabbit corpus cavernosum mediated by nonadrenergic, noncholinergic neurons was attributed to nitric oxide and cyclic guanosine monophosphate (GMP).10 The objective of the present study was to ascertain whether nitric oxide plays a part in similarly mediated relaxation of the corpus cavernosum in humans, and therefore in penile erection.

Methods

Collection of Human Tissue

Portions of corpus cavernosum were obtained from 21 patients at the time of the insertion of a penile prosthesis. These studies were approved by the Human Subjects Protection Committee at our institution, and informed consent was obtained. The tissue was placed in ice-cold Krebs—bicarbonate solution,15 transported to the laboratory, and cut into strips (0.5 by 0.3 by 0.3 cm). Silk ligatures were placed on each strip proximally and distally. We obtained 4 to 12 strips per patient.

Preparation of Tissues for Organ-Bath Experiments

The strips of corpus cavernosum were mounted longitudinally in 25-ml organ-bath chambers with fine Nichrome wires, with the upper wire of each strip attached to a force-displacement transducer (FT03D, Grass Instrument, Quincy, Mass.). Changes in isometric force were measured and recorded on a Grass Polygraph (model 7D). The chambers contained Krebs—bicarbonate solution15 (pH 7.4) at 37°C equilibrated with 95 percent oxygen and 5 percent carbon dioxide. Initially, length—tension relations were determined for each strip obtained from the first six patients. Because little difference was observed among patients, this procedure was performed on only some of the tissue samples from the remaining patients. To adjust the tension to the optimal length for maximal isometric contractions to occur in response to the presence of potassium, the strips were progressively stretched, and contractile responses to potassium chloride (120 mmol per liter) in Krebs—bicarbonate solution were measured, with washing and 15 minutes of equilibration between responses.16 The optimal resting tension for corporal strips prepared in this manner was 1.5 g, and this value did not change for any strip during four to six hours of testing. The maximal contractile tensions that developed in response to potassium chloride ranged from 6 to 8 g. The strips were routinely depolarized with potassium chloride (140 mmol per liter) in Krebs—bicarbonate solution after 60 minutes of equilibration at optimal resting tension; they were then washed and allowed to equilibrate for 30 minutes. This procedure increases and stabilizes the subsequent submaximal contractile responses to phenylephrine, presumably by loading the smooth-muscle cells with calcium; for this reason, it has been used routinely in our laboratory.16 Guanethidine (5 μmol per liter) and atropine (1 μmol per liter) were routinely added to the baths at the start of the 30-minute period of equilibration after potassium depolarization. The strips were subjected to contraction submaximally (to 60 to 75 percent of the size of the maximal contraction induced by potassium chloride) with phenylephrine (1 to 10 μmol per liter), which generated a tension of 4 to 6 g that was maintained reproducibly for the duration of the experiment. Each strip was used in up to four separate rounds of testing, was washed three times with Krebs-bicarbonate solution, and was allowed to equilibrate for 30 minutes between rounds.

Organ-Bath Experiments

The bathing mediums routinely contained, as described above, guanethidine (5 μmol per liter) to produce adrenergic blockade, as assessed by the consistent presence of marked relaxant instead of frequent contractile responses to stimulation by an electrical field, and atropine (1 μmol per liter) to produce cholinergic blockade, as assessed by the abolition of acetylcholine-elicited relaxation.8 , 9 Stimulation was provided with two parallel platinum electrodes 4 to 5 mm apart surrounding the middle portion of the strip and was conducted at sequential frequencies of 4, 2, 4, 8, and 16 Hz as square-wave pulses of 10 V (0.2 msec) delivered for 10-second intervals by a current amplifier and a stimulator (SD9, Grass). The strips were allowed to return to the base-line precontractile tension between the tests at each frequency. The 4-Hz frequency was tested twice during each round of stimulation to ascertain whether the relaxant response at that frequency was highly reproducible over the duration of a given experiment. Variability in the magnitude of relaxation of less than 10 percent was observed at a given frequency for a given strip when the test was repeated throughout a given experiment.

After the completion of the protocol with electrical-field stimulation, either S-nitroso-N-acetylpenicillamine or prostaglandin E₁ (when it was used in a test) was added in increasing concentrations to the precontracted strips. When M&B 22,948, an experimental drug prepared by May and Baker (Dagenham, United Kingdom) was tested, it was added to the strips at a concentration of either 1 or 3 μmol per liter (whichever caused a relaxation of 10 to 15 percent, sufficient to ensure that enough M&B 22,948 had been added). The strips were incubated for 10 minutes before electrical-field stimulation. Subsequently, without the strips being washed, S-nitroso-Nacetylpenicillamine or prostaglandin E₁ was tested. N-nitro-L-arginine (30 μmol per liter) and N-amino-L-arginine (30 μmol per liter), when they were tested, were added to the strips, and after 15 minutes electrical-field stimulation and drug testing were performed. To ascertain whether an excess of arginine could reverse the inhibition of electrically stimulated relaxation caused by the two L-arginine analogues, 300 μmol per liter of L-arginine or its D-enantiomer was added to the medium in the chamber in certain experiments, and stimulation was repeated 15 minutes later. When tetrodotoxin was tested, 1 μmol per liter was added to the precontracted strips five minutes before electrical-field stimulation. To ascertain whether stimulation-induced relaxation was mediated at least in part by the products of cyclooxygenase in certain experiments, strips were incubated with indomethacin (10 μmol per liter) for 30 minutes,16 precontracted, and stimulated with an electrical field. When methylene blue (30 μmol per liter) was tested, it was added 60 minutes before the precontraction of the strips, followed by electrical-field stimulation and drug testing.

Chemicals and Solutions

Phenylephrine hydrochloride, guanethidine sulfate, L-arginine, D-arginine, atropine sulfate, N-nitro-L-arginine, methylene blue, indomethacin, and tetrodotoxin were purchased from Sigma Chemical (St. Louis). Prostaglandin E₁ was obtained from the Upjohn Company (Kalamazoo, Mich.). The water-soluble crystalline hydrochloride salt of N-nitro-L-argimne was prepared by standard chemical procedures. N-amino-L-arginine was synthesized as described elsewhere.17 S-nitroso-N-acetylpenicillamine was prepared, stored, and used as described elsewhere.18 M&B 22,948 was a gift from May and Baker.19 Krebs-bicarbonate solution consisted of the following, expressed as millimoles per liter: sodium chloride, 118; potassium chloride, 4.7; calcium chloride, 1.5; sodium bicarbonate, 25; magnesium sulfate, 1.2; potassium phosphate, 1.2; glucose, 11; and disodium EDTA, 0.023.

Statistical Analysis

The percentage of relaxation refers to the decrease in phenylephrine-induced tone. The mean (±SEM) responses of all the strips of tissue from each patient were recorded for each electrical frequency or drug concentration, and these responses were used as the unit of analysis. The frequency—response and concentration—response curves for a given experiment were compared by a repeated-measures analysis of variance.20 Data analysis indicated that there was a consistent difference between groups at each electrical frequency or drug concentration.

Results

Characteristics of the Subjects

The 21 men ranged in age from 21 to 75 years (average, 60) and had the following diagnoses associated with impotence: radical prostatectomy (four men); diabetes mellitus with hypertension, diabetes mellitus without hypertension, hypertension alone, transurethral prostatectomy, and severe arterial disease (three men each); and Peyronie's disease and quadriplegia (one each).

Characteristics of Electrically Induced Relaxation

Electrical-field stimulation of the strips of corpus cavernosum treated with guanethidine and atropine caused frequency-dependent relaxation (Fig. 1Figure 1Inhibition by W-Nitro-L-Arginine of Electrically Elicited Relaxation of Human Corpus Cavernosum, and Reversal of Inhibition by L-Arginine. and 2Figure 2Inhibition by N-Amino-L-Arginine of Electrically Elicited Relaxation of Human Corpus Cavernosum, and Reversal of Inhibition by L-Arginine.). Tetrodotoxin (1 μmol per liter), a neuronal sodium-channel blocker, abolished the electrically elicited relaxation (not shown), whereas 10 μmol per liter of indomethacin, a cyclooxygenase inhibitor, had no effect (Table 1Table 1Lack of Effect of Indomethacin on Electrically Elicited Relaxation in Samples of Corpus Cavernosum from Five Patients.).

Inhibitory Actions of N-Analogues or L-Arginine

N-nitro-L-arginine and N-amino-L-arginine, structural analogues of L-arginine that inhibit nitric oxide synthase,21 both inhibited electrically elicited relaxation (Fig. 1 and 2). The addition of a 10-fold molar excess of L-arginine (300 μmol per liter) largely reversed the inhibitory actions of both L-arginine analogues (Fig. 1 and 2). In contrast, D-arginine (300 μmol per liter) failed to reverse inhibition by N-nitroL-arginine in experiments in which an identical concentration of L-arginine caused a reversal similar in magnitude to that shown in Figure 1 (as observed in three patients).

Augmenting Action of M&B 22,948

M&B 22,948, a cyclic GMP phosphodiesterase inhibitor,19 augmented the relaxant responses elicited by electrical-field stimulation (Fig. 3Figure 3Enhancement by M&B 22,948 of Electrically Elicited Relaxation of Human Corpus Cavernosum.). S-nitroso-N-acetylpenicillamine, a labile nitroso compound that liberates nitric oxide and elicits pharmacologic actions attributed exclusively to nitric oxide,18 caused a rapid, concentration-dependent relaxation of precontracted strips of corpus cavernosum that was enhanced by M&B 22,948 (Fig. 4Figure 4Enhancement by M&B 22,948 of Relaxation of Human Corpus Cavernosum Elicited by S-Nitroso-N-Acetylpenicillamine.).

Inhibitory Actions of Methylene Blue

Methylene blue, an inhibitor of cytosolic guanylate cyclase,22 inhibited the relaxation of corpus cavernosum smooth muscle elicited by electrical-field stimulation and S-nitroso-N-acetylpenicillamine (Fig. 5Figure 5Inhibition by Methylene Blue of Relaxation of Human Corpus Cavernosum Elicited by Electrical-Field Stimulation and S-Nitroso-N-Acetylpenicillamine.). The relaxation response to S-nitroso-N-acetylpenicillamine was not inhibited by 30 μmol per liter of N-nitro-L-arginine (an inhibitor of the biosynthesis of nitric oxide but not of its action23) in experiments in which N-nitro-L-arginine at this concentration nearly abolished electrically elicited relaxation (observations of four patients).

Preliminary Observations in Men without Impotence

Corporal tissue from two men without impotence and tissue from impotent patients responded similarly with regard to the inhibitory effects of N-nitro-L-arginine and the enhancing effects of M&B 22,948 on electrically elicited relaxation. At a frequency of 8 Hz, N-nitro-L-arginine (30 μmol per liter) caused inhibition ranging from 80 to 86 percent and from 94 to 100 percent, respectively, in the relaxation response of corporal strips from two normal patients and five impotent patients. At a frequency of 2 Hz, M&B 22,948 (1 to 3 μmol per liter) caused increases of 72 to 86 percent and 84 to 96 percent, respectively, in the relaxation response of corporal strips from 2 normal patients and 11 impotent patients.

Discussion

Nitric oxide was first described in 1979 as a potent relaxant of peripheral vascular smooth muscle, with an action mediated by cyclic GMP.24 Acetylcholine was postulated to stimulate the formation of an endothelium-derived relaxing factor,25 which was subsequently identified as being either nitric oxide or a chemically unstable nitroso precursor.26 , 27 Nitric oxide is synthesized from endogenous L-arginine by the nitric oxide synthase system, located in the vascular endothelium,28 and N-substituted analogues of L-arginine, such as N-methyl-, N-nitro-, and N-amino-L-arginine, inhibit nitric oxide synthase20 and endothelium-dependent relaxation.17 , 23

The present study shows that electrical-field stimulation of isolated, precontracted strips of corpus cavernosum from men with impotence causes smooth-muscle relaxation by mechanisms attributed to the formation and release of a relaxing factor with the properties of nitric oxide. Moreover, the addition of nitric oxide, in the form of the labile S-nitroso-Nacetylpenicillamine, caused similar rapid relaxant responses that were inhibited by methylene blue, enhanced by M&B 22,948, and unaffected by N-nitro-L-arginine. M&B 22,948 is a selective inhibitor of cyclic GMP but not cyclic AMP phosphodiesterase,19 as indicated by its capacity to augment the relaxation elicited by electrical-field stimulation and nitric oxide, but not prostaglandin E₁—elicited smooth-muscle relaxation attributed to cyclic AMP formation.29 Although cyclooxygenase products such as prostaglandins may also be involved in electrically elicited relaxation, this does not appear to be the case, because indomethacin at a concentration of 10 μmol per liter (which inhibits cyclooxygenase) had no effect.

The inhibitory effects of N-nitro-L-arginine and N-amino-L-arginine were reversed by the addition of an excess of L-arginine but not of D-arginine, illustrating the enantiomerically selective effect of arginine. N-nitro-L-arginine caused a more potent and effective inhibition of electrically elicited relaxation than N-amino-L-arginine, although the inhibition by both analogues was reversed by the addition of excess L-arginine. Similar observations have been made about other tissues, and the N-methyl analogue appears to behave like the N-amino analogue.17 , 23 The more marked inhibitory action of the N-nitro analogue is probably attributable to the formation of a stronger bond with selective functional groups on the nitric oxide synthase enzyme.

The complete blockade of electrically elicited relaxation of corporal smooth muscle with the addition of tetrodotoxin is consistent with the hypothesis that electrically elicited relaxation is mediated by the nonadrenergic, noncholinergic neuronal pathway.8 , 9 Thus, the present observations suggest that nonadrenergic, noncholinergic neurotransmission is coupled in some manner to the activation of the L-arginine—nitric oxide pathway in human corpus cavernosum. These findings in humans parallel those made in rabbits.10

Nitric oxide may be synthesized and released as a neurotransmitter by the nonadrenergic, noncholinergic neurons. Its labile chemical nature, however, makes it unlikely that nitric oxide could be stored as a preformed neurotransmitter.30 Alternatively, an unidentified neurotransmitter, such as vasoactive intestinal polypeptide, may interact with either endothelial or smooth-muscle cells in the corpus cavernosum to trigger the local formation of nitric oxide.10 Evidence indicates that vascular smooth muscle synthesizes nitric oxide.31 Whether or not the electrically elicited relaxation of corporal smooth muscle is endotheliumdependent is uncertain, but our studies suggest that in rabbit corpus cavernosum the endothelium is not required for such relaxation.10

The present experiments were performed with corporal tissues obtained from men with impotence, so it is appropriate to question whether the proposed mechanism of penile erection applies also to potent men. Preliminary experiments conducted with tissues from two potent men suggest that the L-argininenitric oxide pathway is involved physiologically in mediating the electrically elicited relaxation of corpus cavernosum. The present study, however, was not designed to address any possible differences between impotent and normal patients with regard to the magnitude of the relaxation of corpus cavernosum by elicited electrical-field stimulation. A previous study, however, showed that electrically elicited nonadrenergic, noncholinergic relaxation was impaired in diabetic men with impotence but not in nondiabetic men with impotence.9 Although the present study did not address such differences, the data suggest that the nonadrenergic, noncholinergic L-arginine—nitric oxide pathway may be involved physiologically in mediating penile erection. It is conceivable that impairment of this pathway could account for the impairment in relaxation elicited by electrical-field stimulation that has been described in certain impotent men. Smooth-muscle relaxation is the mechanism by which papaverine and prostaglandin E₁, when injected intracavernosally, cause tumescence in impotent patients.11 , 32 , 33 In view of the previous finding that electrically elicited relaxation of the corpus cavernosum is impaired in men with diabetes and impotence,9 interference with the L-arginine-nitric oxide pathway could be one cause of impotence that is treatable by the administration of direct-acting vasodilators.

Supported in part by grants (HL35014 and HL40922) from the National Institutes of Health and the University Urological Research Foundation.

We are indebted to Dr. J. Fukuto for preparing the N-amino-L-arginine and the salt of N-nitro-L-arginine, and to G. Buga, R. Byrns, Dr. S. Brosman, Dr. W. Casey, C. Forest, Dr. J. Jaffe, Dr. M. Kelly, Dr. L. Marks, and Dr. R. Sugasuwara for their expert assistance.

Source Information

From the Division of Urology, Department of Surgery (J.R., W.J.A., F.J.D.), and the Department of Pharmacology (P.A.B., L.J.I.), University of California School of Medicine, Los Angeles; and the Harbor–UCLA Medical Center, Torrance, Calif. (J.R.). Address reprint requests to Dr. Rajfer at the Division of Urology, Rm. 66–128 CHS, UCLA Medical Center, 10833 Le Conte Ave., Los Angeles, CA 90024.

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