Regulation of intracellular pH in cnidarians: Response to acidosis in Anemonia viridis

FEBS Journal

Volumn 281, Issue 3, 2014, Pages 683-695

  Laurent, Julien ^a   Venn, Alexander ^a,b   Tambutté, Éric ^a,b   Ganot, Philippe ^a   Allemand, Denis ^a,b   Tambutté, Sylvie ^a,b  

^a CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^b CNRS   (France)

Author keywords

Amiloride; Buffer; Cnidarian; EIPA

Indexed keywords

AMMONIUM CHLORIDE; SEA WATER; SODIUM PROTON EXCHANGE PROTEIN;

ACID BASE BALANCE; ACIDIFICATION; ACIDITY; ACIDOSIS; ANEMONIA; ANEMONIA VIRIDIS; ANIMAL CELL; ARTICLE; CELL PH; CONFOCAL MICROSCOPY; ENDODERM; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SYMBIODINIUM; SYMBIONT;

ACTINIARIA; ALGAE; ANEMONE; ANEMONIA VIRIDIS; ANTHOZOA; CNIDARIA; INVERTEBRATA; METAZOA; SYMBIODINIUM SP.;

AMILORIDE; BUFFER; CNIDARIAN; EIPA; NA+/H+ EXCHANGER;

ACID-BASE EQUILIBRIUM; ALLOSTASIS; ALVEOLATA; AMINO ACID SEQUENCE; ANIMALS; CATION TRANSPORT PROTEINS; DATABASES, PROTEIN; HYDROGEN-ION CONCENTRATION; INTRACELLULAR FLUID; ION TRANSPORT; MEDITERRANEAN SEA; MODELS, BIOLOGICAL; PHYLOGENY; PROTEIN ISOFORMS; SALINITY; SEA ANEMONES; SEQUENCE ALIGNMENT; SODIUM-HYDROGEN ANTIPORTER; SYMBIOSIS;

EID: 84897096745     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12614     Document Type: Article

References (63)

1. Weis VM & Allemand D (2009) What determines coral health? Science 324, 1153-1155.
2. Davy SK, Allemand D & Weis VM (2012) Cell biology of Cnidarian-Dinoflagellate symbiosis. Microbiol Mol Biol Rev 76, 229-261.
3. Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez- Lanetty M & Pringle JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23, 369-376.
4. Venn AA, Tambutté É, Holcomb M, Allemand D & Tambutté S (2011) Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6, e20013.
5. Venn AA, Tambutté E, Lotto S, Zoccola D, Allemand D & Tambutté S (2009) Imaging intracellular pH in a reef coral and symbiotic anemone. Proc Natl Acad Sci USA 106, 16574-16579.
6. Boron WF (2004) Regulation of intracellular pH. Physiol Educ 28, 160-179.
7. Casey JR, Grinstein S & Orlowski J (2010) Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11, 50-61.
8. Huynh K, Baker D, Harris R, Church J & Brauner C (2011) Effect of hypercapnia on intracellular pH regulation in a rainbow trout hepatoma cell line, RTH 149. J Comp Physiol B 181, 883-892.
9. Murer H, Hopfer U & Kinne R (1976) Sodium/proton antiport in brushborder-membrane vesicles isolated from rat small intestine and kidney. Biochemistry 154, 597-604.
10. Orlowski J & Grinstein S (2004) Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflügers Archiv 447, 549-565.
11. Furimsky M, Moon TW & Perry SF (1999) Intracellular pH regulation in hepatocytes isolated from three Teleost species. J Exp Zool 284, 361-367.
12. Venn AA, Loram JE & Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59, 1069-1080.
13. Yellowlees D, Rees TAV & Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell Environ 31, 679-694.
14. Laurent J, Tambutté S, Tambutté É, Allemand D & Venn A (2013) The influence of photosynthesis on host intracellular pH in scleractinian corals. J Exp Biol 216, 1398-1404.
15. Furla P, Bénazet-Tambutté S, Jaubert J & Allemand D (1998) Functional polarity of the tentacle of the sea anemone Anemonia viridis: role in inorganic carbon acquisition. Am J Physiol 274, 303-310.
16. Gattuso JP & Hansson L (2011) Ocean Acidification. Oxford University Press, Oxford.
17. Bénazet-Tambutté S, Allemand D & Jaubert J (1996) Inorganic carbon supply to symbiont photosynthesis of the sea anemone, Anemonia viridis: role of the oral epithelial layers. Symbiosis 20, 199-217.
18. Ganot P, Moya A, Magnone V, Allemand D, Furla P & Sabourault C (2011) Adaptations to endosymbiosis in a Cnidarian-Dinoflagellate association: differential gene expression and specific gene duplications. PLoS Genet 7, e1002187.
19. Laurent J, Tambutté S, Tambutté É, Allemand D & Venn A (2012) The influence of photosynthesis on host intracellular pH in scleractinian corals. J Exp Biol 216, 1398-1404.
20. Bergman JA, McAteer JA, Evan AP & Soleimani M (1991) Use of the pH-sensitive dye BCECF to study pH regulation in cultured human kidney proximal tubule cells. J Tiss Cult Methods 13, 205-209.
21. Sarangarajan R, Shumaker H, Soleimani M, Le Poole C & Boissy RE (2001) Molecular and functional characterization of sodium-hydrogen exchanger in skin as well as cultured keratinocytes and melanocytes. Biochim Biophys Acta 1511, 181-192.
22. Stumpp M, Hu MY, Melzner F, Gutowska MA, Dorey N, Himmerkus N, Holtmann WC, Dupont ST, Thorndyke MC & Bleich M (2012) Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc Natl Acad Sci USA 109, 18192-18197.
23. Tufts BL & Boutilier RG (1989) The absence of rapid chloride/bicarbonate exchange in lamprey erythrocytes: implications for CO2 transport and ion distributions between plasma and erythrocytes in the blood of Petromyzon marinus. J Exp Biol 144, 565-576.
24. Bouyer P, Bradley SR, Zhao J, Wang W, Richerson GB & Boron WF (2004) Effect of extracellular acid- base disturbances on the intracellular pH of neurones cultured from rat medullary raphe or hippocampus. J Physiol 559, 85-101.
25. Nimer NA, Brownlee C & Merrett MJ (1994) Carbon dioxide availability, intracellular pH and growth rate of the coccolithophore Emiliania huxleyi. Mar Ecol Prog Ser 109, 257-262.
26. Michaelidis B, Ouzounis C, Paleras A & Pörtner HO (2005) 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.
27. Loiselle F & Casey J (2010) Measurement of intracellular pH. In Membrane Transporters in Drug Discovery and Development (Yan Q, ed.) pp. 311-331, Humana Press, New York.
28. Boron WF, McCormick WC & Roos A (1979) pH regulation in barnacle muscle fibers: dependence on intracellular and extracellular pH. Am J Physiol 237, C185-C193.
29. Nordström T, Shrode LD, Rotstein OD, Romanek R, Goto T, Heersche JNM, Manolson MF, Brisseau GF & Grinstein S (1997) Chronic extracellular acidosis induces plasmalemmal vacuolar type H+ ATPase activity in osteoclasts. J Biol Chem 272, 6354-6360.
30. Burton RF (1978) Intracellular buffering. Respir Physiol 33, 51-58.
31. Pörtner H-O (1990) Determination of intracellular buffer values after metabolic inhibition by fluoride and nitrilotriacetic acid. Respir Physiol 81, 275-288.
32. Thomas RC (1976) The effect of carbon dioxide on the intracellular pH and buffering power of snail neurones. J Physiol 255, 715-735.
33. Wiseman RW & Ellington WR (1989) Intracellular buffering capacity in molluscan muscle: superfused muscle versus homogenates. Physiol Zool 62, 541-558.
34. Zange J, Grieshaber MK & Jans AW (1990) The regulation of intracellular pH estimated by 31P-NMR spectroscopy in the anterior byssus retractor muscle of Mytilus Edulis. J Exp Biol 150, 95-109.
35. Sterling D & Casey JR (1999) Transport activity of AE3 chloride/bicarbonate anion-exchange proteins and their regulation by intracellular pH. Biochem J 344, 221-229.
36. Bevensee MO & Boron WF (2008) Control of intracellular pH. In Seldin and Giebisch's The Kidney: Physiology and Pathophysiology, 4th edn (Alpern R & Hebert S, eds), pp. 1429-1480. Academic Press, New York.
37. Aickin CC & Thomas RC (1977) An investigation of the ionic mechanism of intracellular pH regulation in mouse soleus muscle fibres. J Physiol 273, 295-316.
38. Boron WF & Boulpaep EL (1983) Intracellular pH regulation in the renal proximal tubule of the salamander Na+-H+ exchange. J Gen Physiol 81, 29-52.
39. Moody WJ (1981) The ionic mechanism of intracellular pH regulation in crayfish neurones. J Physiol 316, 293-308.
40. Vigne P, Frelin C, Cragoe EJ & Lazdunski M (1984) Structure-activity relationships of amiloride and certain of its analogues in relation to the blockade of the Na+/ H+ exchange system. Mol Pharmacol 25, 131-136.
41. Ahearn GA, Mandal PK & Mandal A (2001) Biology of the 2Na+/1H+ antiporter in invertebrates. J Exp Zool 289, 232-244.
42. Aronson PS (1985) Kinetic properties of the plasma membrane Na+-H+ exchanger. Annu Rev Physiol 47, 545-560.
43. Frelin C, Vigne P, Ladoux A & Lazdunski M (1988) The regulation of the intracellular pH in cells from vertebrates. Eur J Biochem 174, 3-14.
44. Grinstein S, Rotin D & Mason MJ (1989) Na+/H+ exchange and growth factor-induced cytosolic pH changes. Role in cellular proliferation. Biochim Biophys Acta 988, 73-97.
45. Hoffmann EK & Simonsen LO (1989) Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol Rev 69, 315-382.
46. Noel J & Pouyssegur J (1995) Hormonal regulation, pharmacology, and membrane sorting of vertebrate Na+/H+ exchanger isoforms. Am J Physiol 268, C283- C296.
47. Wakabayashi S, Shigekawa M & Pouyssegur J (1997) Molecular physiology of vertebrate Na+/H+ exchangers. Physiol Rev 77, 51-74.
48. Slepkov E & Fliegel L (2002) Structure and function of the NHE1 isoform of the Na+/H+ exchanger. Biochem Cell Biol 80, 499-508.
49. Slepkov ER, Rainey JK, Sykes BD & Fliegel L (2007) Structural and functional analysis of the Na+/H+ exchanger. Biochem J 401, 623-633.
50. Roos A & Boron WF (1981) Intracellular pH. Physiol Rev 61, 296-434.
51. Boron WF & De Weer P (1976) Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors. J Gen Physiol 67, 91-112.
52. Boron WF (1977) Intracellular pH transients in giant barnacle muscle fibers. Am J Physiol 233, C61-C73.
53. Waugh A & Grant A (2007) Anatomy and Physiology in Health and Illness, 10th edn. Churchill Livingstone Elsevier, New York. p. 22.
54. Venn AA, Tambutté E, Holcomb M, Laurent J, Allemand D & Tambutté S (2013) Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc Natl Acad Sci USA 110, 1634-1639.
55. Barott KL, Helman Y, Haramaty L, Barron ME, Hess KC, Buck J, Levin LR & Tresguerres M (2013) High adenylyl cyclase activity and in vivo cAMP fluctuations in corals suggest central physiological role. Sci Rep 3, 1379.
56. Dickson A, Sabine C & Christian J, eds (2007) Guide to Best Practices for Ocean CO2 Measurements, PICES Special Publication 3. North Pacific Marine Science Organization, Sidney, BC, Canada.
57. US Department of Energy (1994) Handbook of Methods for the Analysis of the Various Parameters of the Carbon Dioxide System in Sea Water, version 2, ORNL/ CDIAC-74, eds Dickson AG & Goyet C (Oak Ridge National Laboratory/Carbon Dioxide Information Analysis Center, Oak Ridge, TN).
58. Pelletier G, Lewis E & Wallace D (2007) COSYS.xls: A Calculator for the CO2 System in Seawater for Microsoft Excel/VBA. Washington State Department for Ecology, Olympia, WA; Brookhaven National Laboratory, Upton, NY.
59. Mehrbach C, Culberson CH, Hawley JE & Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18, 897-907.
60. Dickson AG & Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Pt I 34, 1733-1743.
61. Bénazet-Tambutté S (1996) Le tissu oral des anthozoaires: fonctionnement et rôle dans l'association symbiotique, PhD thesis, Université d'Aix-Marseille II, Fr.
62. Frank HA & Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63, 257-264.
63. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ & Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150, 76-85.