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Biol. Bull. 209: 6-10. (August 2005)
© 2005 Marine Biological Laboratory

Sodium Nitroprusside Potentiates Hydrogen-Sulfide-Induced Contractions in Body Wall Muscle From a Marine Worm

David Julian1,*, Jennifer Statile2, Troy A. Roepke2 and Alissa J. Arp2

1 Department of Zoology, University of Florida, Gainesville, Florida 32611
2 Romberg Tiburon Center for Environmental Studies, San Francisco State University, San Francisco, California 94920

* To whom correspondence should be addressed. E-mail: djulian{at}ufl.edu

Abbreviations: ACh, acetylcholine • H2S, hydrogen sulfide • 5HT, 5-hydroxytryptamine • NaHS, sodium hydrosulfide • NO, nitric oxide • PLP, pyridoxal-5'-phosphate • SNP, sodium nitroprusside

Hydrogen sulfide (H2S) at concentrations of about 0.05 to 1 mmol · l–1 appears to function as a gasotransmitter in vertebrates, analogous to nitric oxide (NO) and carbon monoxide (1–5), but the actions of H2S in invertebrate tissue have not been well studied. In this study, we investigated the role of H2S in modulating body wall muscle tone in the marine echiuran worm Urechis caupo (Echiuridae). We first determined that U. caupo body wall homogenates produce H2S upon addition of L-cysteine and pyridoxal-5'-phosphate (PLP), and that the rate is increased by addition of 2-mercaptoethanol, suggesting the presence of an activated L-serine sulfhydrase pathway. We then measured the contractile response of U. caupo body wall circular muscle strips to sodium hydrosulfide (NaHS)—which produces H2S in solution— and the NO donor sodium nitroprusside (SNP), both with and without subsequent application of acetylcholine (ACh). We found that NaHS alone stimulated contraction in muscle strips equivalent to about one-third the force of ACh alone, whereas SNP alone had no effect on muscle tone. However, simultaneous addition of NaHS with SNP elicited a much stronger contraction, reaching more than twice that of ACh alone, which could be increased further by subsequent application of ACh.

Free H2S is present in tissues of both vertebrates (1, 6, 7) and invertebrates (8, 9) at concentrations as high as 0.02 to 0.07 mmol · l–1. This finding was initially surprising, given the well-known toxicity of H2S, which includes inhibition of mitochondrial cytochrome c oxidase at low micromolar levels (10). H2S can be produced from L-cysteine by pyridoxal-5'-phosphate-dependent enzymes, including cystathionine ß-synthase (CBS) and cystathionine {gamma}-lyase (CSE). Endogenous enzymatic production has been shown in tissues from mammals (1, 11–13), the clam Tapes philippinarum and the annelid Arenicola marina (14), and the clam Mercenaria mercenaria (15).

The identification of both H2S and enzymatic pathways for H2S production in tissues has stimulated an ongoing search for potential actions of H2S as an endogenous signaling molecule. In mammalian smooth muscle, 0.025 to 0.1 mmol · l–1 H2S elicits concentration-dependent relaxation in aorta, ileum, portal vein, and vas deferens (11, 16, 17) and decreases spontaneous contractility in uterus (18). In mammalian cardiac muscle, H2S decreases contractility both in vivo and in vitro (12). The net cardiovascular effect of H2S in mammals is decreased blood pressure, similar to the action of NO. At least some of these actions of H2S are likely mediated through direct activation of ATP-sensitive K+ (KATP) channels (13). Two studies have addressed the action of H2S on nonmammalian vertebrates (5, 7), with the most recent of these being a careful, phylogenetic survey of responses among the vertebrates (5), and have shown that many smooth muscles have complex, multiphasic responses to H2S (e.g., relaxation-constriction-relaxation).

In contrast to recent work on mammalian smooth and cardiac muscle, there has been little information about potential signaling actions of H2S in invertebrate muscle. At concentrations above about 5 mmol · l–1, H2S inhibits body wall muscle contraction in U. caupo, but this is more likely a toxic effect (19). H2S at 0.05 to 0.1 mmol · l–1 also impairs or prevents associative learning and long-term memory in the freshwater snail Lymnaea (20), but whether this affected muscle tone was not tested. However, Gainey and Greenberg (15) reported that, in branchial muscles of the clam M. mercenaria, NaHS potentiates the contractile action of 5-hydroxytryptamine (5HT), although it does not directly affect muscle tone. This effect on 5HT-induced contractions is similar to the action of NO on 5HT-induced contractions in the same muscle. The effect is seen at NaHS concentrations as low as 10 nmol · l–1, with a maximal effect at 1 µmol · l–1, and appears to act through a soluble guanylate cyclase (sGC) cascade. In mammals, by comparison, 0.3 to 1 mmol · l–1 H2S can almost completely reverse the response to exogenous ACh and norepinephrine in guinea pig ileum and portal vein but not thoracic aorta, and H2S greatly enhances the smooth muscle relaxant effect of SNP on thoracic aorta (11). This latter effect was also noted over a decade earlier in guinea pig ileum by Kruszyna et al. (21), but this was prior to the recognition that H2S and NO have signaling functions.

In this study, we investigated H2S production and the effects of NaHS on muscle contraction in vitro in Urechis caupo Fisher and MacGinitie, 1928, which is a large (60 g or more) worm that inhabits U-shaped burrows in mudflats along the California coast (22). We collected specimens of U. caupo by hand at low tides during winter at Pillar Point Harbor in San Mateo County, California. The worms were maintained unfed in filtered, aerated, recirculating seawater for no more than 3 weeks before they were used for experiments. To confirm that U. caupo tissues have the capacity to produce H2S, body wall homogenates were prepared and assayed for H2S production in the presence and absence of 10 mmol · l–1 L-cysteine with 2 mmol · l–1 PLP, as described previously for Tapes philippinarum (14). U. caupo body wall tissue alone produced no detectable H2S, but this increased to 0.2 nmol H2S g–1 · min–1 (n = 2) when L-cysteine and PLP were added. These results are comparable to previously reported production rates for adductor muscle, siphon, and gill tissue from T. philippinarum and body wall from Arenicola marina (14). Addition of 2.5 mmol · l–1 2-mercaptoethanol increased H2S production to 0.5 nmol · g–1 · min–1, suggesting the presence of an "activated L-serine sulfhydrase pathway," similar to tissues of T. philippinarum, but in contrast to A. marina, which does not show evidence of this pathway in body wall (14).

To investigate the effect of NaHS and SNP on muscle contraction, strips of body wall circular muscle were mounted to a force transducer, and muscle tension was recorded during bath exposure to 0.1 mmol · l–1 ACh to elicit contraction (23), 1 mmol · l–1 NaHS and 1 mmol · l–1 SNP, as well as simultaneous application of NaHS and SNP (1 mmol · l–1 each) followed by ACh. In 19 of 22 strips, ACh alone elicited a slow contraction with a mean force of 3.3 g ± 0.56 (SD) g (Fig. 1A). The remaining 3 strips did not respond to ACh. NaHS alone elicited a contraction in 5 of 8 strips, although the response was smaller than with ACh (Fig. 1B). Therefore, unlike mammalian smooth muscle, in which H2S causes relaxation, U. caupo muscle contracts in response to H2S (as NaHS). The only previous demonstration of H2S-induced muscle contraction is the triphasic response of trout branchial artery (7). In contrast to NaHS, SNP had no effect on muscle tone (Fig. 1C). However, simultaneous application of NaHS and SNP elicited a much larger contraction than from NaHS alone, and this was further increased by subsequent application of ACh (Fig. 1D).



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  		Figure 1. Contraction force in strips of Urechis caupo body wall circular muscle in vitro in response to bath application of acetylcholine (ACh), sodium hydrosulfide (NaHS), and sodium nitroprusside (SNP). The scale bar indicates tension (vertical axis) and time (horizontal axis). (A) Reference contraction in response to 0.1 mmol · l–1 ACh (at arrow). (B) Small, extended contraction in response to 1 mmol · l–1 NaHS (at arrow) (C) Application of 1 mmol · l–1 SNP had no effect on muscle tension. (D) Simultaneous application of 1 mmol · l–1 SNP and 1 mmol · l–1 NaHS (at first arrow) caused a contraction almost equivalent to that of ACh alone, while subsequent application of 0.1 mmol · l–1 ACh (at second arrow) elicited an even larger contraction. Methods: Circular muscle strips of uniform length, thickness, and width were cut from the body wall of each worm, using a tissue chopper consisting of 20 razor blades bolted together with 5 mm between each blade. The strips were immediately placed in aerated buffer (37 g · l–1 Instant Ocean, 50 mmol · l–1 Na-Hepes, and 1.0 g · l–1 dextrose, pH 7.4) at 9°C for no more than 4 h before being used. For each trial, a single strip was mounted between stainless steel hooks and connected to an isometric force transducer (S10, World Precision Instruments) on a micromanipulator. The strip was then lowered into a chamber containing 6 ml of aerated buffer at room temperature (20–22 °C) and slowly stretched to a preload tension of 2.75 g. Digital recording was then initiated at 5 Hz, and ACh, NaHS, and SNP were added alone or in combination, as indicated in the text. Throughout each trial, the chamber solution was kept well stirred with a magnetic stirrer. Stock solutions of 10 mmol · l–1 NaHS and 10 mmol · l–1 SNP were prepared fresh in buffer, stored on ice (in darkness for SNP), and used within 2 h.

 
The possibility of an interaction was investigated further by testing muscle strips at 16 combinations of NaHS with SNP, each at four levels (0, 0.01, 0.1, and 1 mmol · l–1). For each muscle strip, 0.1 mmol · l–1 ACh was also added after the contraction from NaHS with SNP reached a plateau (or after it was clear there would be no contraction). We found that the lowest concentration of NaHS (0.01 mmol · l–1) had no effect on muscle tension, whereas 0.1 and 1 mmol · l–1 NaHS produced a contraction equivalent in force to about 0.3 times that of ACh alone (Fig. 2A, note the "0 mM SNP" bars at each NaHS concentration), with a range of 0.03 to 0.9. In contrast, SNP alone had no effect at any concentration (Fig. 2A; i.e., cluster of bars "0 mM NaHS"). However, simultaneous application of NaHS with SNP elicited a strong contraction. At 1 mmol · l–1 NaHS, the average force (relative to 0.1 mmol · l–1 ACh) was 2.4 ± 0.7 and 2.7 ± 0.19 (SD) for 0.1 and 1 mmol · l–1 SNP, respectively (Fig. 2A; note the shaded bars in cluster at "1.0 mM NaHS"). To test for interactions, the data were analyzed by two-factor within-subjects ANOVA, followed by the Tukey HSD multiple comparisons test (Statistica ver. 5.5; Statsoft, Inc., Tulsa, OK). The effect of NaHS on force was significant (P = 0.0063, F3 = 8.1), whereas the effect of SNP alone was not (P = 0.15, F3 = 2.3), and there was a significant interaction between NaHS and SNP (P = 0.032, F3 = 2.5). When ACh was added to the strips, the resulting contraction had a tendency to increase with increasing SNP but not with increasing NaHS (Fig. 2B), but statistical analyses (performed as above) did not detect any significant differences among the treatments (probably due at least in part to the large variation in the response to ACh and the comparatively small sample size). By comparison, in rat aortic helical strips precontracted with norepinephrine, the vasorelaxant effect of SNP is enhanced with NaHS (11), whereas in rings of the same tissue precontracted with phenylephrine, NaHS inhibits the effect of SNP (16); the reason for the discrepancy in these two studies is unclear (16). It should also be noted that although the NaHS concentrations necessary to produce an effect in U. caupo body wall were similar to (11) or only slightly higher than (16) that required to contract rat aorta and smooth muscle of other vertebrate vessels (5), the SNP concentrations necessary for interaction with NaHS in U. caupo muscle were at least an order of magnitude higher than that required in rat aorta.



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  		Figure 2. Contraction force in strips of Urechis caupo body wall circular muscle in vitro in response to simultaneous bath application of sodium nitroprusside (SNP; 0.01, 0.1, and 1 mmol · l–1) and sodium hydrosulfide (NaHS; 0.01, 0.1, and 1 mmol · l–1), followed by 0.1 mmol · l–1 acetylcholine (ACh). Data are presented as mean ± SEM, with 4 independent replicates for each of the 16 NaHS with SNP combinations (A) Change in muscle tension immediately following simultaneous addition of NaHS and SNP. Contraction force is relative to the force elicited by 0.01 mmol · l–1 ACh alone in reference strips. (B) Change in muscle tension following addition of ACh to strips pre-contracted by NaHS and SNP. Force is presented as the tension generated in addition to that elicited by NaHS and SNP, and is relative to the force elicited by 0.01 mmol · l–1 ACh alone in reference strips. Methods: Strips from 4 animals were prepared as described in Figure 1, with each strip being used for only one treatment. The order of treatments was randomized for each animal, and every 5th strip was exposed to ACh alone as a reference (≥ 4 reference strips per animal). For analysis, the contraction force of each NaHS with SNP strip was normalized to the average force of the reference ACh strips for that animal.

 
The data in this study indicate that a homogenate of U. caupo body wall tissue produces H2S upon addition of cysteine, and that NaHS elicits a contraction in body wall muscle that is potentiated by SNP. The nature of the interaction between SNP and NaHS in this study and in three studies of mammalian smooth muscle (11, 16, 21) is not known. However, since SNP alone had no effect on body wall muscle tone in U. caupo, the interaction between NaHS and SNP is not simply additive, as may occur in rat aorta (11). SNP donates NO in solution, raising the possibility that H2S and NO act on separate signaling receptor sites (e.g., 4, 13, 24). On the other hand, SNP reacts directly with thiols in vitro to form nitrosothiol complexes and free radicals via nucleophilic attack on the NO ligand, which is accompanied by a color change to purple-red (25). Presumably, this is also the basis of NO release in vivo, for which potential thiols include cysteine, homocysteine, and glutathione (25, 26), but could also include H2S. Therefore, NaHS may enhance the release of NO from SNP. Furthermore, reaction of SNP with thiols may also produce S-nitrosothiols (26), which can act as storage and transport forms of NO (27) and may also directly modulate vessel tone in mammals (28). This suggests that reaction of NaHS with SNP may not only increase the release of NO, but may additionally produce S-nitrosothiols that then release NO over time and may also act directly. In support of this possibility, an aerated solution of NaHS and SNP (1 mmol · l–1 each) retains its capacity to modulate trout vascular smooth muscle tone for 30 min or more, even after the purple-red color has disappeared (R. A. Dombkowski and K. R. Olson, University of Notre Dame, pers. comm.).

Interestingly, H2S signaling in Mercenaria mercenaria appears to have a seasonal component (15); the effect of NaHS on 5HT action was present in February and March but absent in August, whereas H2S production was highest in summer months. We only tested the effect of NaHS on U. caupo collected in winter, so it is unknown whether the response would have differed in other seasons. It is clear, however, that the apparent potentiation of NaHS by SNP in U. caupo differs in at least two ways from the effect of NaHS on M. mercenaria (15). First, no direct effect of NaHS on muscle tone was observed in M. mercenaria, whereas NaHS alone induced contraction in U. caupo. Second, NaHS and NO can each potentiate 5HT alone in M. mercenaria, whereas in U. caupo there was no significant action of NaHS or SNP, either together or alone, on the action of ACh. Nonetheless, taken together, our data provide strong evidence that H2S acts as an endogenous signaling transmitter in invertebrates, and that H2S—whether alone or in combination with ACh or 5HT—has the capacity to stimulate contraction, which is opposite to the relaxation elicited by H2S in mammalian smooth muscle. It is worth noting, however, that both U. caupo and M. mercenaria are found in habitats with environmental H2S, and indeed multiple "sulfide-detoxification mechanisms" have been described in U. caupo (29, 30) and other so-called "sulfide-adapted" animals (31). Whether other invertebrates respond to endogenous H2S in the same way as sulfide-adapted invertebrates remains to be determined.


   Acknowledgments
 
This research was supported by NIH MBRS S06 6M 52588-01-7 to AJA. All experiments complied with University of Florida and San Francisco State University Institutional Animal Care and Use Committee requirements. We thank SE Wohlgemuth, JL Joyner-Matos, and two anonymous reviewers for helpful comments.


   Footnotes
 
Received 14 March 2005; accepted 4 June 2005.


   Literature Cited
TOP
 Literature Cited
 

  1. Abe, K., and H. Kimura. 1996. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 16(3): 1066–1071.
  2. Kimura, H. 2002. Hydrogen sulfide as a neuromodulator. Mol. Neurobiol. 26: 13–19.[ISI][Medline]
  3. Wang, R. 2002. Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 16: 1792–1798.[Abstract/Free Full Text]
  4. Boehning, D., and S. H. Snyder. 2003. Novel neural modulators. Annu. Rev. Neurosci. 26: 105–131.[ISI][Medline]
  5. Dombkowski, R. A., M. J. Russell, A. A. Schulman, M. M. Doellman, and K. R. Olson. 2005. Vertebrate phylogeny of hydrogen sulfide vasoactivity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288: R243–252.[Abstract/Free Full Text]
  6. Warenycia, M. W., L. R. Goodwin, C. G. Benishin, R. J. Reiffenstein, D. M. Francom, J. D. Taylor, and F. P. Dieken. 1989. Acute hydrogen sulfide poisoning: demonstration of selective uptake of sulfide by the brainstem by measurement of brain sulfide levels. Biochem. Pharmacol. 38: 973–981.[ISI][Medline]
  7. Dombkowski, R. A., M. J. Russell, and K. R. Olson. 2004. Hydrogen sulfide as an endogenous regulator of vascular smooth muscle tone in trout. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286: R678–685.[Abstract/Free Full Text]
  8. Hauschild, K., and M. K. Grieshaber. 1997. Oxygen consumption and sulfide detoxification in the lugworm Arenicola marina (L.) at different ambient oxygen partial pressures and sulfide concentrations. J. Comp. Physiol. B 167: 378–388.
  9. Wohlgemuth, S., A. C. Taylor, and M. K. Grieshaber. 2000. Ventilatory and metabolic responses to hypoxia and sulphide in the lugworm, Arenicola marina (L.). J. Exp. Biol. 203: 3177–3188.[Abstract]
  10. National Research Council Subcommittee on Medical and Biologic Effects of Environmental Pollutants. 1979. Hydrogen Sulfide. University Park Press, Baltimore, MD.
  11. Hosoki, R., N. Matsuki, and H. Kimura. 1997. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem. Biophys. Res. Commun. 237: 527–531.[ISI][Medline]
  12. Geng, B., J. Yang, Y. Qi, J. Zhao, Y. Pang, J. Du, and C. Tang. 2004. H2S generated by heart in rat and its effects on cardiac function. Biochem. Biophys. Res. Commun. 313: 362–368.[ISI][Medline]
  13. Zhao, W., J. Zhang, Y. Lu, and R. Wang. 2001. The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO (Eur. Mar. Biol. Organ.) J. 20: 6008–6016.
  14. Julian, D., J. L. Statile, S. E. Wohlgemuth, and A. J. Arp. 2002. Enzymatic hydrogen sulfide production in marine invertebrate tissues. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 133:105–115.[Medline]
  15. Gainey, L. F., and M. J. Greenberg. 2005. Hydrogen sulfide is synthesized in the gills of the clam Mercenaria mercenaria and acts seasonally to modulate branchial muscle contraction. Biol. Bull. 209: 11–20.[Abstract/Free Full Text]
  16. Zhao, W., and R. Wang. 2002. H2S-induced vasorelaxation and underlying cellular and molecular mechanisms. Am. J. Physiol. Heart Circ. Physiol. 283: H474–480.[Abstract/Free Full Text]
  17. Teague, B., S. Asiedu, and P. K. Moore. 2002. The smooth muscle relaxant effect of hydrogen sulphide in vitro: evidence for a physiological role to control intestinal contractility. Br. J. Pharmacol. 137: 11–20.
  18. Sidhu, R., M. Singh, G. Samir, and R. J. Carson. 2001. L-cysteine and sodium hydrosulphide inhibit spontaneous contractility in isolated pregnant rat uterine strips in vitro. Pharmacol. Toxicol. 88: 198–203.[ISI][Medline]
  19. Julian, D., W. E. Dalia, and A. J. Arp. 1998. Neuromuscular sensitivity to hydrogen sulfide in the marine invertebrate Urechis caupo. J. Exp. Biol. 201: 1393–1403.[Abstract]
  20. Rosenegger, D., S. Roth, and K. Lukowiak. 2004. Learning and memory in Lymnaea are negatively altered by acute low-level concentrations of hydrogen sulphide. J. Exp. Biol. 207: 2621–2630.[Abstract/Free Full Text]
  21. Kruszyna, H., R. Kruszyna, and R. P. Smith. 1985. Cyanide and sulfide interact with nitrogenous compounds to influence the relaxation of various smooth muscles. Proc. Soc. Exp. Biol. Med. 179: 44–49.[Abstract]
  22. Arp, A. J., B. M. Hansen, and D. Julian. 1992. The burrow environment and coelomic fluid characteristics of the echiuran worm Urechis caupo from three northern California population sites. Mar. Biol. 13: 613–623.
  23. Muneoka, Y., and M. Kamura. 1982. Actions of noradrenaline and some other biogenic amines on the body-wall muscles of an echiuroid, Urechis unicinctus. Comp. Biochem. Physiol. C 72: 281–287.
  24. Kimura, H. 2000. Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem. Biophys. Res. Commun. 267: 129–133.[ISI][Medline]
  25. Szacilowski, K., A. Wanat, A. Barbieri, E. Wasielewska, M. Witko, G. Stochel, and Z. Stasicka. 2002. Reactions of the [Fe(CN)5NO]2– complex with biologically relevant thiols. New J. Chem. 26: 1495–1502.
  26. Grossi, L., and S. D’Angelo. 2005. Sodium nitroprusside: mechanism of NO release mediated by sulfhydryl-containing molecules. J. Med. Chem. 48: 2622–2626.[ISI][Medline]
  27. Rafikova, O., R. Rafikov, and E. Nudler. 2002. Catalysis of S-nitrosothiols formation by serum albumin: the mechanism and implication in vascular control. Proc. Natl. Acad. Sci. USA 99: 5913–5918.[Abstract/Free Full Text]
  28. Batenburg, W. W., R. Popp, I. Fleming, R. de Vries, I. M. Garrelds, P. R. Saxena, and A. H. Danser. 2004. Bradykinin-induced relaxation of coronary microarteries: S-nitrosothiols as EDHF? Br. J. Pharmacol. 142: 125–135.[ISI][Medline]
  29. Arp, A. J., J. G. Menon, and D. Julian. 1995. Multiple mechanisms provide tolerance to environmental sulfide in Urechis caupo. Am. Zool. 35: 132–144.
  30. Julian, D., S. L. Wieting, S. L. Seto, M. R. Bogan, and A. J. Arp. 1999. Thiosulfate elimination and permeability in a sulfide-adapted marine invertebrate. Physiol. Biochem. Zool. 72: 416–425.[ISI][Medline]
  31. Grieshaber, M. K., and S. Völkel. 1998. Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu. Rev. Physiol. 60: 33–53.[ISI][Medline]



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