Established and potential physiological roles of bicarbonatesensing soluble adenylyl cyclase (sAC) in aquatic animals

Journal of Experimental Biology

Volumn 217, Issue 5, 2014, Pages 663-672

  Tresguerres, Martin ^a   Barott, Katie L ^a   Barron, Megan E ^a   Roa, Jinae N ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Acid base; CAMP; Carbonic anhydrase; PH sensing; Proton pump; V ATPase

Indexed keywords

ADENYLATE CYCLASE; BICARBONATE; CARBONATE DEHYDRATASE; CYCLIC AMP; PROTON PUMP;

ACID/BASE; ANIMAL; INVERTEBRATE; METABOLISM; PH SENSING; REVIEW; V-ATPASE; VERTEBRATE;

ACID/BASE; CAMP; CARBONIC ANHYDRASE; PH SENSING; PROTON PUMP; V-ATPASE;

ADENYLATE CYCLASE; ANIMALS; BICARBONATES; INVERTEBRATES; VERTEBRATES;

EID: 84896897975     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.086157     Document Type: Review

References (112)

1. Acin-Perez, R., Salazar, E., Kamenetsky, M., Buck, J., Levin, L. R. and Manfredi, G. (2009). Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab. 9, 265-276.
2. Appukuttan, A., Kasseckert, S. A., Micoogullari, M., Flacke, J.-P., Kumar, S., Woste, A., Abdallah, Y., Pott, L., Reusch, H. P. and Ladilov, Y. (2012). Type 10 adenylyl cyclase mediates mitochondrial Bax translocation and apoptosis of adult rat cardiomyocytes under simulated ischaemia/reperfusion. Cardiovasc. Res. 93, 340-349.
3. Barott, K. L., Helman, Y., Haramaty, L., Barron, M. E., Hess, K. C., Buck, J., Levin, L. R. and Tresguerres, M. (2013). High adenylyl cyclase activity and in vivo cAMP fluctuations in corals suggest central physiological role. Sci Rep 3, 1379.
4. Barron, M. E., Roa, J. N. B. and Tresguerres, M. (2012). Pacific oyster mantle, gill and hemocytes express the bicarbonate-sensing enzyme soluble adenylyl cyclase. FASEB J. 26, 1070.2.
5. Beltrán, C., Vacquier, V. D., Moy, G., Chen, Y., Buck, J., Levin, L. R. and Darszon, A. (2007). Particulate and soluble adenylyl cyclases participate in the sperm acrosome reaction. Biochem. Biophys. Res. Commun. 358, 1128-1135.
6. Bettice, J. A., Owens, D. and Riley, S. (1984). The effects of hypocapnia on intracellular pH and bicarbonate. Respir. Physiol. 55, 121-130.
7. Bookbinder, L. H., Moy, G. W. and Vacquier, V. D. (1990). Identification of sea urchin sperm adenylate cyclase. J. Cell Biol. 111, 1859-1866.
8. Bracho, G. E., Fritch, J. J. and Tash, J. S. (1998). Identification of flagellar proteins that initiate the activation of sperm motility in vivo. Biochem. Biophys. Res. Commun. 242, 231-237.
9. Braun, T. (1974). Evidence for multiple, cell specific, distinctive adenylate cyclase systems in rat testis. Curr. Top. Mol. Endocrinol. 1, 243-264.
10. Braun, T. (1975). The effect of divalent cations on bovine spermatozoal adenylate cyclase activity. J. Cyclic Nucleotide Res. 1, 271-281.
11. Braun, T. (1990). Inhibition of the soluble form of testis adenylate cyclase by catechol estrogens and other catechols. Proc. Soc. Exp. Biol. Med. 194, 58-63.
12. Braun, T. (1991). Purification of soluble form of adenylyl cyclase from testes. Methods Enzymol. 195, 130-136.
13. 2+- sensitive, 'soluble' adenylate cyclase in rat testis. Proc. Natl. Acad. Sci. USA 72, 1097-1101.
14. Brown, D. and Wagner, C. A. (2012). Molecular mechanisms of acid-base sensing by the kidney. J. Am. Soc. Nephrol. 23, 774-780.
15. Buck, J., Sinclair, M. L., Schapal, L., Cann, M. J. and Levin, L. R. (1999). Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc. Natl. Acad. Sci. USA 96, 79-84.
16. Byrne, R. A. and Dietz, T. H. (2006). Ionic and acid-base consequences of exposure to increased salinity in the zebra mussel, Dreissena polymorpha. Biol. Bull. 211, 66-75.
17. Carvalho, E. S., Gregório, S. F., Power, D. M., Canário, A. V. and Fuentes, J. (2012). Water absorption and bicarbonate secretion in the intestine of the sea bream are regulated by transmembrane and soluble adenylyl cyclase stimulation. J. Comp. Physiol. B 182, 1069-1080.
18. Chaloupka, J. A., Bullock, S. A., Iourgenko, V., Levin, L. R. and Buck, J. (2006). Autoinhibitory regulation of soluble adenylyl cyclase. Mol. Reprod. Dev. 73, 361-368.
19. Chen, Y., Cann, M. J., Litvin, T. N., Iourgenko, V., Sinclair, M. L., Levin, L. R. and Buck, J. (2000). Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289, 625-628.
20. Chen, H., Guo, J. H., Lu, Y. C., Ding, G. L., Yu, M. K., Tsang, L. L., Fok, K. L., Liu, X. M., Zhang, X. H., Chung, Y. W. et al. (2012a). Impaired CFTR-dependent amplification of FSH-stimulated estrogen production in cystic fibrosis and PCOS. J. Clin. Endocrinol. Metab. 97, 923-932.
21. Chen, J., Levin, L. R. and Buck, J. (2012b). Role of soluble adenylyl cyclase in the heart. Am. J. Physiol. 302, H538-H543.
22. Choi, H. B., Gordon, G. R. J., Zhou, N., Tai, C., Rungta, R. L., Martinez, J., Milner, T. A., Ryu, J. K., McLarnon, J. G., Tresguerres, M. et al. (2012). Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl cyclase. Neuron 75, 1094-1104.
23. Cooper, D. M. (2003). Regulation and organization of adenylyl cyclases and cAMP. Biochem. J. 375, 517-529.
24. Corredor, R. G., Trakhtenberg, E. F., Pita-Thomas, W., Jin, X., Hu, Y. and Goldberg, J. L. (2012). Soluble adenylyl cyclase activity is necessary for retinal ganglion cell survival and axon growth. J. Neurosci. 32, 7734-7744.
25. Fabbri, E. and Capuzzo, A. (2010). Cyclic AMP signaling in bivalve molluscs: an overview. J. Exp. Zool. A 313, 179-200.
26. tm1Lex 'knockout' mice. PLoS ONE 3, e3251.
27. Flacke, J. P., Kempkes, H., Appukuttan, A., Palisaar, R. J., Noldus, J., Robinson, B. D., Reusch, H. P., Zippin, J. H. and Ladilov, Y. (2013). Type 10 soluble adenylyl cyclase is overexpressed in prostate carcinoma and controls proliferation of prostate cancer cells. J. Biol. Chem. 288, 3126-3135.
28. Furla, P., Galgani, I., Durand, I. and Allemand, D. (2000). Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J. Exp. Biol. 203, 3445-3457.
29. Garbers, D. L. and Kopf, G. S. (1980). The regulation of spermatozoa by calcium cyclic nucleotides. Adv. Cyclic Nucleotide Res. 13, 251-306.
30. Geng, W., Wang, Z., Zhang, J., Reed, B. Y., Pak, C. Y. and Moe, O. W. (2005). Cloning and characterization of the human soluble adenylyl cyclase. Am. J. Physiol. 288, C1305-C1316.
31. Gilmour, K. M., Bayaa, M., Kenney, L., McNeill, B. and Perry, S. F. (2007). Type IV carbonic anhydrase is present in the gills of spiny dogfish (Squalus acanthias). Am. J. Physiol. 292, R556-R567.
32. +-ATPase apical accumulation in kidney intercalated cells is regulated by PKA and AMP-activated protein kinase. Am. J. Physiol. 298, F1162-F1169.
33. Grosell, M. (2011). Intestinal anion exchange in marine teleosts is involved in osmoregulation and contributes to the oceanic inorganic carbon cycle. Acta Physiol. (Oxf.) 202, 421-434.
34. Guillou, J. L., Nakata, H. and Cooper, D. M. (1999). Inhibition by calcium of mammalian adenylyl cyclases. J. Biol. Chem. 274, 35539-35545.
35. Gutowska, M. A., Melzner, F., Langenbuch, M., Bock, C., Claireaux, G. and Pörtner, H. O. (2010). Acid-base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. J. Comp. Physiol. B 180, 323-335.
36. Hanoune, J. and Defer, N. (2001). Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol. 41, 145-174.
37. Heisler, N. (1988). Acid-base regulation. In Physiology of Elasmobranch Fishes (ed. T. J. Shuttleworth), pp. 215-252. Berlin: Springer:Verlag.
38. Hess, K. C., Jones, B. H., Marquez, B., Chen, Y., Ord, T. S., Kamenetsky, M., Miyamoto, C., Zippin, J. H., Kopf, G. S., Suarez, S. S. et al. (2005). The 'soluble' adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev. Cell 9, 249-259.
39. Hobe, H., Wood, C. M. and Wheatly, M. G. (1984). The mechanisms of acid-base and ionoregulation in the freshwater rainbow trout during environmental hyperoxia and subsequent normoxia. I. Extra-and intracellular acid-base status. Respir. Physiol. 55, 139-154.
40. Jaiswal, B. S. and Conti, M. (2001). Identification and functional analysis of splice variants of the germ cell soluble adenylyl cyclase. J. Biol. Chem. 276, 31698-31708.
41. Jaiswal, B. S. and Conti, M. (2003). Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc. Natl. Acad. Sci. USA 100, 10676-10681.
42. Kamenetsky, M., Middelhaufe, S., Bank, E. M., Levin, L. R., Buck, J. and Steegborn, C. (2006). Molecular details of cAMP generation in mammalian cells: a tale of two systems. J. Mol. Biol. 362, 623-639.
43. Kolodecik, T. R., Shugrue, C. A., Thrower, E. C., Levin, L. R., Buck, J. and Gorelick, F. S. (2012). Activation of soluble adenylyl cyclase protects against secretagogue stimulated zymogen activation in rat pancreaic acinar cells. PLoS ONE 7, e41320.
44. Kumar, S., Kostin, S., Flacke, J. P., Reusch, H. P. and Ladilov, Y. (2009). Soluble adenylyl cyclase controls mitochondria-dependent apoptosis in coronary endothelial cells. J. Biol. Chem. 284, 14760-14768.
45. Lannig, G., Eilers, S., Pörtner, H. O., Sokolova, I. M. and Bock, C. (2010). Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas-changes in metabolic pathways and thermal response. Mar. Drugs 8, 2318-2339.
46. 2 levels. Am. J. Respir. Cell Mol. Biol. 48, 626-634.
47. Lee, Y. S., Tresguerres, M., Hess, K., Marmorstein, L. Y., Levin, L. R., Buck, J. and Marmorstein, A. D. (2011). Regulation of anterior chamber drainage by bicarbonate-sensitive soluble adenylyl cyclase in the ciliary body. J. Biol. Chem. 286, 41353-41358.
48. Linder, J. U. (2006). Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation. Cell. Mol. Life Sci. 63, 1736-1751.
49. Linder, J. U. and Schultz, J. E. (2008). Versatility of signal transduction encoded in dimeric adenylyl cyclases. Curr. Opin. Struct. Biol. 18, 667-672.
50. Litvin, T. N., Kamenetsky, M., Zarifyan, A., Buck, J. and Levin, L. R. (2003). Kinetic properties of 'soluble' adenylyl cyclase. Synergism between calcium and bicarbonate. J. Biol. Chem. 278, 15922-15926.
51. Lodish, H. F. (1999). Molecular Cell Biology. New York, NY: Scientific American Books.
52. Lomovatskaya, L. A., Romanenko, A. S., Filinova, N. V. and Salyaev, R. K. (2008). Detection of soluble adenylyl cyclase isoforms in plants. Dokl. Biochem. Biophys. 420, 124-126.
53. 2+ in the haemolymph: implications on the calcification physiology in Anodonta cygnea. J. Comp. Physiol. B 179, 279-286.
54. Magro, C. M., Crowson, A. N., Desman, G. and Zippin, J. H. (2012a). Soluble adenylyl cyclase antibody profile as a diagnostic adjunct in the assessment of pigmented lesions. Arch. Dermatol. 148, 335-344.
55. Magro, C. M., Yang, S.-E., Zippin, J. H. and Zembowicz, A. (2012b). Expression of soluble adenylyl cyclase in lentigo maligna: use of immunohistochemistry with anti-soluble adenylyl cyclase antibody (R21) in diagnosis of lentigo maligna and assessment of margins. Arch. Pathol. Lab. Med. 136, 1558-1564.
56. Mancebo, M., Treviño, M., Crespo, C. and Espinosa, J. (1991). Adenylate cyclase activity in Mytilus galloprovincialis Lmk: characteristics of the enzyme from mantle tissue. J. Exp. Zool. A 258, 174-180.
57. 2 acquisition systems in response to CO2 concentration. Photosynth. Res. 109, 191-203.
58. Michaelidis, B., Haas, D. and Grieshaber, M. K. (2005a). Extracellular and intracellular acid-base status with regard to the energy metabolism in the oyster Crassostrea gigas during exposure to air. Physiol. Biochem. Zool. 78, 373-383.
59. Michaelidis, B., Ouzounis, C., Paleras, A. and Portner, H. O. (2005b). Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar. Ecol. Prog. Ser. 293, 109-118.
60. Middelhaufe, S., Leipelt, M., Levin, L. R., Buck, J. and Steegborn, C. (2012). Identification of a haem domain in human soluble adenylate cyclase. Biosci. Rep. 32, 491-499.
61. Moore, S. W., Lai Wing Sun, K., Xie, F., Barker, P. A., Conti, M. and Kennedy, T. E. (2008). Soluble adenylyl cyclase is not required for axon guidance to netrin-1. J. Neurosci. 28, 3920-3924.
62. Morisawa, M. and Ishida, K. (1987). Short-term changes in levels of cyclic AMP, adenylate cyclase, and phosphodiesterase during the initiation of sperm motility in rainbow trout. J. Exp. Zool. 242, 199-204.
63. Morisawa, S. and Morisawa, M. (1988). Induction of potential for sperm motility by bicarbonate and pH in rainbow trout and chum salmon. J. Exp. Biol. 136, 13-22.
64. Nomura, M. and Vacquier, V. D. (2006). Proteins associated with soluble adenylyl cyclase in sea urchin sperm flagella. Cell Motil. Cytoskeleton 63, 582-590.
65. Nomura, M., Beltrán, C., Darszon, A. and Vacquier, V. D. (2005). A soluble adenylyl cyclase from sea urchin spermatozoa. Gene 353, 231-238.
66. Pastor-Soler, N., Beaulieu, V., Litvin, T. N., Da Silva, N., Chen, Y., Brown, D., Buck, J., Levin, L. R. and Breton, S. (2003). Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J. Biol. Chem. 278, 49523-49529.
67. Pastor-Soler, N. M., Hallows, K. R., Smolak, C., Gong, F., Brown, D. and Breton, S. (2008). Alkaline pH-and cAMP-induced V-ATPase membrane accumulation is mediated by protein kinase A in epididymal clear cells. Am. J. Physiol. 294, C488-C494.
68. Paunescu, T. G., Da Silva, N., Russo, L. M., McKee, M., Lu, H. A., Breton, S. and Brown, D. (2008). Association of soluble adenylyl cyclase with the V-ATPase in renal epithelial cells. Am. J. Physiol. 294, F130-F138.
69. Piermarini, P. M., Verlander, J. W., Royaux, I. E. and Evans, D. H. (2002). Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch. Am. J. Physiol. 283, R983-R992.
70. Ramos, L. S., Zippin, J. H., Kamenetsky, M., Buck, J. and Levin, L. R. (2008). Glucose and GLP-1 stimulate cAMP production via distinct adenylyl cyclases in INS-1E insulinoma cells. J. Gen. Physiol. 132, 329-338.
71. Richards, J. G., Heigenhauser, G. J. F. and Wood, C. M. (2003). Exercise and recovery metabolism in the Pacific spiny dogfish (Squalus acanthias). J. Comp. Physiol. B 173, 463-474.
72. Roa, J. N. B., Barron, M. E. and Tresguerres, M. (2012). Bicarbonate-sensing soluble adenylyl cyclase in elasmobranch and teleost fishes. FASEB J. 26, 442-447.
73. Roelofs, J. and Van Haastert, P. J. (2002). Deducing the origin of soluble adenylyl cyclase, a gene lost in multiple lineages. Mol. Biol. Evol. 19, 2239-2246.
74. Romanenko, A. S., Lomovatskaya, L. A., Filinova, N. V., Kopytchuk, V. N. and Salyaev, R. K. (2008). Intracellular localization of 'soluble' adenylate cyclase in potato plants. Doklady Biological Sciences 422, 328-329.
75. Schmid, A., Sutto, Z., Schmid, N., Novak, L., Ivonnet, P., Horvath, G., Conner, G., Fregien, N. and Salathe, M. (2010). Decreased soluble adenylyl cyclase activity in cystic fibrosis is related to defective apical bicarbonate exchange and affects ciliary beat frequency regulation. J. Biol. Chem. 285, 29998-30007.
76. Seamon, K. B. and Daly, J. W. (1981). Forskolin: a unique diterpene activator of cyclic AMP-generating systems. J. Cyclic Nucleotide Res. 7, 201-224.
77. Seamon, K. B., Padgett, W. and Daly, J. W. (1981). Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc. Natl. Acad. Sci. USA 78, 3363-3367.
78. Shuttleworth, T. J., Thompson, J., Munger, R. S. and Wood, C. M. (2006). A critical analysis of carbonic anhydrase function, respiratory gas exchange, and the acid-base control of secretion in the rectal gland of Squalus acanthias. J. Exp. Biol. 209, 4701-4716.
79. Steegborn, C., Litvin, T. N., Hess, K. C., Capper, A. B., Taussig, R., Buck, J., Levin, L. R. and Wu, H. (2005a). A novel mechanism for adenylyl cyclase inhibition from the crystal structure of its complex with catechol estrogen. J. Biol. Chem. 280, 31754-31759.
80. Steegborn, C., Litvin, T. N., Levin, L. R., Buck, J. and Wu, H. (2005b). Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment. Nat. Struct. Mol. Biol. 12, 32-37.
81. Strobel, A., Bennecke, S., Leo, E., Mintenbeck, K., Pörtner, H. O. and Mark, F. C. (2012). Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2. Front. Zool. 9, 28.
82. +-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias). J. Exp. Biol. 208, 345-354.
83. Tresguerres, M., Katoh, F., Orr, E., Parks, S. K. and Goss, G. G. (2006a). Chloride uptake and base secretion in freshwater fish: a transepithelial ion-transport metabolon? Physiol. Biochem. Zool. 79, 981-996.
84. +-ATPase to the basolateral membrane in the Pacific spiny dogfish (Squalus acanthias): a role in base secretion. J. Exp. Biol. 209, 599-609.
85. +-ATPase translocation during blood alkalosis in dogfish gills: interaction with carbonic anhydrase and involvement in the postfeeding alkaline tide. Am. J. Physiol. 292, R2012-R2019.
86. Tresguerres, M., Buck, J. and Levin, L. (2010a). Physiological carbon dioxide, bicarbonate, and pH sensing. Pflügers Arch. 460, 953-964.
87. -] in the marine teleost intestine is mediated by soluble adenylyl cyclase. Am. J. Physiol. 299, R62-R71.
88. Tresguerres, M., Parks, S. K., Salazar, E., Levin, L. R., Goss, G. G. and Buck, J. (2010c). Bicarbonate-sensing soluble adenylyl cyclase is an essential sensor for acid/base homeostasis. Proc. Natl. Acad. Sci. USA 107, 442-447.
89. Tresguerres, M., Levin, L. R. and Buck, J. (2011). Intracellular cAMP signaling by soluble adenylyl cyclase. Kidney Int. 79, 1277-1288.
90. Valbonesi, P., Caselli, F., Capuzzo, A. and Fabbri, E. (2004). Modulation of adenyl cyclase activity in the gills of Tapes philippinarum. J. Exp. Zool. A 301, 952-960.
91. Walsh, P. J., Blackwelder, P., Gill, K. A., Danulat, E. and Mommsen, T. P. (1991). Carbonate deposits in marine fish intestines: a new source of biomineralization. Limnol. Oceanogr. 36, 1227-1232.
92. Walsh, P. J., Kajimura, M., Mommsen, T. P. and Wood, C. M. (2006). Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland. J. Exp. Biol. 209, 2929-2938.
93. Wang, H. and Storm, D. R. (2003). Calmodulin-regulated adenylyl cyclases: cross-talk and plasticity in the central nervous system. Mol. Pharmacol. 63, 463-468.
94. Wang, T., Busk, M. and Overgaard, J. (2001). The respiratory consequences of feeding in amphibians and reptiles. Comp. Biochem. Physiol. 128A, 533-547.
95. Weiss, S. and Drummond, G. I. (1985). Biochemical properties of adenylate cyclase in the gill of Aplysia californica. Comp. Biochem. Physiol. 80B, 251-255.
96. 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 87, 965-1010.
97. Wilson, R. W., Wilson, J. M. and Grosell, M. (2002). Intestinal bicarbonate secretion by marine teleost fish-why and how? Biochim. Biophys. Acta 1566, 182-193.
98. Wilson, R. W., Millero, F. J., Taylor, J. R., Walsh, P. J., Christensen, V., Jennings, S. and Grosell, M. (2009). Contribution of fish to the marine inorganic carbon cycle. Science 323, 359-362.
99. Wong, W. and Scott, J. D. (2004). AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell Biol. 5, 959-970.
100. Wood, C. M., Turner, J. D., Munger, R. S. and Graham, M. S. (1990). Control of ventilation in the hypercapnic skate Raja ocellata: II. Cerebrospinal fluid and intracellular pH in the brain and other tissues. Respir. Physiol. 80, 279-297.
101. Wood, C. M., Kajimura, M., Mommsen, T. P. and Walsh, P. J. (2005). Alkaline tide and nitrogen conservation after feeding in an elasmobranch (Squalus acanthias). J. Exp. Biol. 208, 2693-2705.
102. Wood, C. M., Bucking, C., Fitzpatrick, J. and Nadella, S. (2007a). The alkaline tide goes out and the nitrogen stays in after feeding in the dogfish shark, Squalus acanthias. Respir. Physiol. Neurobiol. 159, 163-170.
103. Wood, C. M., Munger, R. S., Thompson, J. and Shuttleworth, T. J. (2007b). Control of rectal gland secretion by blood acid-base status in the intact dogfish shark (Squalus acanthias). Respir. Physiol. Neurobiol. 156, 220-228.
104. Wood, C. M., Kajimura, M., Mommsen, T. P. and Walsh, P. J. (2008). Is the alkaline tide a signal to activate metabolic or ionoregulatory enzymes in the dogfish shark (Squalus acanthias)? Physiol. Biochem. Zool. 81, 278-287.
105. Wood, C. M., Schultz, A. G., Munger, R. S. and Walsh, P. J. (2009). Using omeprazole to link the components of the post-prandial alkaline tide in the spiny dogfish, Squalus acanthias. J. Exp. Biol. 212, 684-692.
106. Zaccolo, M. (2009). cAMP signal transduction in the heart: understanding spatial control for the development of novel therapeutic strategies. Br. J. Pharmacol. 158, 50-60.
107. Zaccolo, M., Di Benedetto, G., Lissandron, V., Mancuso, L., Terrin, A. and Zamparo, I. (2006). Restricted diffusion of a freely diffusible second messenger: mechanisms underlying compartmentalized cAMP signalling. Biochem. Soc. Trans. 34, 495-497.
108. Zhu, X., Mahairas, G., Illies, M., Cameron, R. A., Davidson, E. H. and Ettensohn, C. A. (2001). A large-scale analysis of mRNAs expressed by primary mesenchyme cells of the sea urchin embryo. Development 128, 2615-2627.
109. Zilli, L., Schiavone, R., Storelli, C. and Vilella, S. (2008). Molecular mechanisms determining sperm motility initiation in two sparids (Sparus aurata and Lithognathus mormyrus). Biol. Reprod. 79, 356-366.
110. Zippin, J. H., Chen, Y., Nahirney, P., Kamenetsky, M., Wuttke, M. S., Fischman, D. A., Levin, L. R. and Buck, J. (2003). Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J. 17, 82-84.
111. Zippin, J. H., Farrell, J., Huron, D., Kamenetsky, M., Hess, K. C., Fischman, D. A., Levin, L. R. and Buck, J. (2004). Bicarbonate-responsive 'soluble' adenylyl cyclase defines a nuclear cAMP microdomain. J. Cell Biol. 164, 527-534.
112. Zippin, J. H., Chadwick, P. A., Levin, L. R., Buck, J. and Magro, C. M. (2010). Soluble adenylyl cyclase defines a nuclear cAMP microdomain in keratinocyte hyperproliferative skin diseases. J. Invest. Dermatol. 130, 1279-1287.