Search:
Computing and Library Services - delivering an inspiring information environment

Activation of the newly discovered cyclostome rennin-angiotensin system in the river lamprey Lampetra fluviatilis

Brown, Anne J., Cobb, Christopher S., Frankling, Susan C. and Rankin, J. Cliff (2005) Activation of the newly discovered cyclostome rennin-angiotensin system in the river lamprey Lampetra fluviatilis. Journal of Experimental Biology, 208. pp. 223-232. ISSN 0022-0949

[img] PDF
Restricted to Registered users only

Download (209kB)

    Abstract

    This study describes the first investigations of the physiological signals involved in activating the newly discovered cyclostome renin–angiotensin system (RAS) and its role in the river lamprey Lampetra fluviatilis. Experimental manipulation showed that volume depletion (removal of 40% blood volume) rapidly activated the RAS of lampreys acclimated to water at 576 mOsm kg–1 (21 p.p.t.), significantly increasing plasma angiotensin concentrations after 30 min and 60 min. In agreement with these results, a rapid change in environmental salinity (758 mOsm kg–1 to freshwater (FW) and FW to 605 mOsm kg–1), resulted in a rapid decrease and increase in plasma [angiotensin], respectively. Intraperitoneal (i.p.) injection of FW-acclimated river lampreys with 1% body mass by volume of nominally isosmotic saline (120 mmol l–1 NaCl; 233 mOsm kg–1) resulted in a significant decrease in the plasma angiotensin concentration within 15 min. In contrast, i.p. injection of hyperosmotic saline (4 mol l–1 NaCl) at 1% body mass by volume, which significantly increased plasma osmolality, had no significant effect on plasma [angiotensin], suggesting that volume/pressure receptors and osmoreceptors interact in regulating the lamprey RAS. These results indicate an important role for volume/pressor receptors, as in teleosts, but with an additional osmoreceptor mechanism, such that circulatory [angiotensin] is determined by interaction of volume/pressure and osmoreceptors and their relative sensitivities. The volume/pressure sensitivity is in keeping with the recent evidence of a vasoconstrictor action of homologous lamprey angiotensin and provides evidence that the fundamental role of the RAS in maintaining volume and pressure is an ancient function conserved over 500 million years of vertebrate evolution.

    Item Type: Article
    Additional Information: Published by © The Company of Biologists
    Uncontrolled Keywords: renin–angiotensin system, river lamprey, Lampetra fluviatilis, plasma angiotensin, salinity adaptation, volume regulation
    Subjects: G Geography. Anthropology. Recreation > G Geography (General)
    G Geography. Anthropology. Recreation > GE Environmental Sciences
    Schools: School of Applied Sciences
    References:

    Anderson, W. G., Cerra, M. C., Wells, A., Tierney, M. L., Tota, B., Takei,
    Y. and Hazon, N. (2001). Angiotensin and angiotensin receptors in
    cartilaginous fishes. Comp. Biochem. Physiol. 128A, 31-40.
    Arnold-Reed, D. E and Balment, R. J. (1994). Peptide-hormones influence
    in vitro interrenal secretion of cortisol in the trout, Oncorhynchus mykiss.
    Gen. Comp. Endocrinol. 96, 85-91.
    Aust, J. G. (2002). Molecular and physiological investigations of fish renin
    angiotensin systems. PhD thesis, University of Exeter, UK.
    Bailey, J. R. and Randall, D. J. (1981). Renal perfusion pressure and renin
    secretion in the rainbow trout, Salmo gairdneri. Can. J. Zool. 59, 1220-1226.
    Balment, R. J., Warne, J. M. and Takei, Y. (2003). Isolation, synthesis, and
    biological activity of flounder [Asn1, Ile5, Thr9] angiotensin I. Gen. Comp.
    Endocrinol. 130, 92-98.
    Bernier, N. J. and Perry, S. F. (1999). Cardiovascular effects of angiotensin-
    II-mediated adrenaline release in rainbow trout Oncorhynchus mykiss. J.
    Exp. Biol. 202, 55-66.
    Bernier, N. J., Kaiya, H., Takei, Y. and Perry, S. F. (1999). Mediation of
    humoral catecholamine secretion by the renin-angiotensin system in
    hypotensive rainbow trout (Oncorhynchus mykiss). J. Endocrinol. 160, 351-
    363.
    Blair-West, J. R., Cohlan, J. P., Denton, D. A., Gibson, A. P., Oddie, C.
    J., Sawyer, W. H. and Scroggins, B. A. (1977). Plasma renin activity and
    blood corticosteroids in the Australian lungfish Neoceratodus forsteri. J.
    Endocrinol. 74, 137-142.
    Brown, J. A. and Balment, R. J. (1997). Teleost renal function: regulation
    by arginine vasotocin and by angiotensins. In Ionic Regulation in Animals
    (ed. N. Hazon, F. B. Eddy and G. Flik), pp. 150-154. Heidelberg: Springer
    Verlag.
    Brown, J. A. and Rankin, J. C. (1999). Lack of glomerular intermittency in
    the river lamprey Lampetra fluviatilis acclimated to sea water and following
    acute transfer to iso-osmotic brackish water. J. Exp. Biol. 202, 939-946.
    Brown, J. A., Oliver, J. A., Henderson, I. W. and Jackson B. A. (1980).
    Angiotensin and single nephron glomerular function in the rainbow trout
    Salmo gairdneri. Am. J. Physiol. 239, R509-R514.
    Brown, J. A., Paley, R. K., Amer, S. and Aves, S. J. (2000). Evidence for
    an intrarenal renin-angiotensin system in the rainbow trout, Oncorhynchus
    mykiss. Am. J. Physiol. 278, R1685-R1691.
    Butler, D. G. and Oudit, G. Y. (1995). Angiotensin-I and -III-mediated
    cardiovascular responses in the freshwater North American eel, Anguilla
    rostrata: Effect of Phe8 deletion. Gen. Comp. Endocrinol. 97, 259-269.
    Butler, D. G. and Zhang, D. H. (2001). Corpuscles of Stannius secrete renin
    or an isorenin that regulates cardiovascular function in freshwater North
    American eel, Anguilla anguilla LeSueur. Gen. Comp. Endocrinol. 124,
    199-217.
    Conlon, J. M., Yano, K. J. and Olson, K. R. (1996). Production of
    [Asn1,Val5] angiotensin II and [Asp1,Val5] angiotensin II in kallikreintreated
    trout plasma (T60K). Peptides 17, 527-530.
    Evans, D. H. (1993). Osmotic and ionic regulation. In Physiology of Fishes
    (ed. D. H. Evans), pp. 315-342. Boca Raton, FL: CRC Press.
    Galli, S. M. and Phillips, M. I. (1996). Interactions of angiotensin II and atrial
    natriuretic peptide in the brain: fish to rodent. Proc. Soc. Exp. Biol. Med.
    213, 128-137.
    Hardisty, M. W. (1979). Biology of Cyclostomes. Chapman and Hall, London.
    Hasegawa, Y., Watanabe, T. X., Nakajima, T. and Sokabe, H. (1984).
    Chemical structure of angiotensin formed by incubating plasma with
    corpuscles of Stannius in the Japanese goosefish Lophius litulon. Gen.
    Comp. Endocrinol. 54, 264-269.
    Henderson, I. W., Brown, J. A. and Balment, R. J. (1993). The reninangiotensin
    system and volume homeostasis. In New Insights in Vertebrate
    Kidney Function (ed. J. A. Brown, R. J. Balment and J. C. Rankin), pp. 311-
    350. Cambridge: Cambridge University Press.
    Khosla, M. C., Nishimura, H., Hasegawa, Y. and Bumpus. F. M. (1985).
    Identification and synthesis of [1-asparagine, 5-valine, 9-glycine]
    angiotensin I produced from plasma of American eel Anguilla rostrata.
    Gen. Comp. Endocrinol. 57, 223-233.
    Klett, C. P. R. and Granger, J. P. (2001). Physiological elevation in plasma
    angiotensinogen increases blood pressure. Am. J. Physiol. 281, R1437-
    R1441.
    Kobayashi, H. and Takei, Y. (1996). The renin-angiotensin system –
    comparative aspects. In Zoophysiology, vol. 35. Berlin: Springer Verlag.
    Logan, A. D., Morris, R. and Rankin, J. C. (1980). A micropuncture study
    of kidney function in the river lamprey Lampetra fluviatilis adapted to sea
    water. J. Exp. Biol. 88, 239-247.
    McVicar, A. J. and Rankin, J. C. (1983). Renal function in unanaesthetised
    river lampreys (Lampetra fluviatilis L.): effects of anaesthesia, temperature
    and environmental salinity. J. Exp. Biol. 105, 351-362.
    McVicar, A. J. and Rankin, J. C. (1985). Dynamics of glomerular filtration
    in the river lamprey, Lampetra fluviatilis (L.) Am. J. Physiol. 249, F132-
    138.
    Nishimura, H. (1985). Evolution of the renin-angiotensin system and its role
    in control of cardiovascular function in fishes. In Evolutionary Biology of
    Primitive Fishes (ed. R. E. Foreman, J. M. Gorbman, J. M. Dodd and R.
    Olsson), pp. 275-293. New York: Plenum Press.
    Nishimura, H. (2004). Phylogeny and ontogeny of the renin-angiotensin
    system. In Handbook of Experimental Pharmacology Vol 163/I Angiotensin,
    Vol. I (ed. T. Unger and B. A. Schölkens), pp. 31-70. Berlin: Springer-
    Verlag.
    Nishimura, H. and Bailey R. J. (1982). Intrarenal renin-angiotensin system
    in primitive vertebrates. Kid. Int. Suppl. 12, S185-S192.
    Nishimura, H. and Ogawa, M. (1973). The renin-angiotensin system in
    fishes. Amer. Zool. 13, 823-838.
    Nishimura, H., Oguri, M., Ogawa, M., Sokabe, H. and Imai, I. (1970).
    Absence of renin in kidneys of elasmobranchs and cyclostomes. Am. J.
    Physiol. 218, 911-915.
    Nishimura, H., Lunde, I. G. and Zucker, A. (1979). Renin response to
    hemorrhage and hypotension in the aglomerular toadfish Opsanus tau. Am.
    J. Physiol. 6, H105-H111.
    Olson, K. R. (1992). Blood and extracellular fluid volume regulation: role of
    the renin-angiotensin, kallikrein-kinin system and atrial peptides. In Fish
    Physiology, Vol 12B (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp.
    135-254. London: Academic Press.
    Peti-Peterdi, J., Fintha, A., Fuson, A. L., Tousson, A. and Chow, R. H.
    (2004). Real-time imaging of renin release in vitro. Am. J. Physiol. 287,
    F329-F335.
    Rankin, J. C. (1996). Osmoregulatory physiology of adult lampreys. In The
    Physiology of Migrating Fish (ed. S. McCormick, M. Sheridan, R. Patiño
    and D. Mackinlay), pp. 131-135. San Francisco: American Fisheries
    Society.
    Rankin, J. C. (1997). Osmotic and ionic regulation in cyclostomes. In Ionic
    Regulation in Animals (ed. N. Hazon, F. B. Eddy and G. Flik), pp. 50-69.
    Berlin: Springer Verlag.
    Rankin, J. C. (2002). Drinking in hagfishes and lampreys. In Osmoregulation
    and Drinking in Vertebrates (ed. N. Hazon and G. Flik), pp 1-17. Oxford:
    BIOS Scientific Publishers Ltd.
    Rankin, J. C., Cobb, C. S., Frankling, S. C. and Brown, J. A. (2001).
    Circulating angiotensins in the river lamprey, Lampetra fluviatilis,
    acclimated to freshwater and seawater: possible involvement in the
    regulation of drinking. Comp. Biochem. Physiol. 129B, 311-318.
    Rankin, J. C., Watanabe, T. X., Nakajima, K., Broadhead, C. and Takei,
    Y. (2004). Identification of angiotensin I in a cyclostome, Lampetra
    fluviatilis. Zool. Sci. 21, 173-179.
    Takei, Y., Hasegawa, Y., Watanabe, T. X., Nakajima, K. and Hazon, N.
    (1993). A novel angiotensin I isolated from an elasmobranch fish. J.
    Endocrinol. 139, 281-285.
    Takei, Y., Joss, J. M. P., Kloas, W. and Rankin, J. C. (2004). Identification
    of angiotensin I in several vertebrate species: Its structural and functional
    evolution. Gen. Comp. Endocrinol. 135, 286-292.
    Tierney, M. L., Cramb, G. and Hazon, N. (1995a). Stimulation of the reninangiotensin
    system and drinking by papaverine in the seawater eel, Anguilla
    anguilla. J. Fish Biol. 46 721-724.
    Tierney, M. L. Luke, G., Cramb, G. and Hazon, N. (1995b). The role of
    the renin-angiotensin system in the control of blood-pressure and drinking
    in the European eel, Anguilla anguilla. Gen. Comp. Endocrinol. 100, 39-48.
    Thorson, T. B. (1959). Partitioning of body water in sea lamprey. Science
    130, 99-100.
    Wilkie, M. P., Turnbull, S., Bird, J., Wang, Y. S., Claude, J. F. and
    Youson, J. H. (2004). Lamprey parasitism of sharks and teleosts: high
    capacity urea excretion in an extant vertebrate relic. Comp. Biochem.
    Physiol. 138A, 485-492.
    Yamaguchi, K. (1981). Effects of water deprivation on immunoreactive
    angiotensin II levels in plasma, cerebroventricular perfusate and
    hypothalamus of the rat. Acta Endocrinol. (Copenh.) 97, 137-144.

    Depositing User: Sara Taylor
    Date Deposited: 20 Dec 2007
    Last Modified: 28 Jul 2010 19:20
    URI: http://eprints.hud.ac.uk/id/eprint/221

    Document Downloads

    Downloader Countries

    More statistics for this item...

    Item control for Repository Staff only:

    View Item

    University of Huddersfield, Queensgate, Huddersfield, HD1 3DH Copyright and Disclaimer All rights reserved ©