Home LiteratureArticle Details
PMID: 6885905 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Transient increase in calcium efflux accompanies fertilization in Chlamydomonas.

The Journal of cell biology ·Vol. 97 ·No. 2 ·1983-08-00 ·Pages 397-404

Bloodgood RA, Levin EN

Abstract

Mating in Chlamydomonas is a complex process initiated by contact of gametic flagellar surfaces, resulting in transmission of a signal from the flagella to the cell bodies. This signal triggers later events of cell wall loss, mating structure activation, and cell-cell fusion. Little is known about the nature of the signal or the role of Ca in these events. It was found that extracellular Ca is not necessary for successful mating in Chlamydomonas. However, cells will take up Ca from the medium in a linear manner for many hours and will accumulate micromolar concentrations, presumably by sequestering Ca within intracellular storage sites. If gametic cells of one mating type (preloaded with 45Ca) are mated with gametes of the opposite mating type (preloaded with unlabeled calcium), there is a rapid, transient increase in calcium efflux rate (20 times that of the control) that lasts approximately 6 min. This effect is not associated with cell-cell fusion, since the same observation is made if (+) gametes preloaded with 45-Ca are agglutinated by isolated flagella from (-) gametes preloaded with unlabeled Ca. Other experiments have shown that the increased efflux rate is not a simple consequence of cell wall release. Ca efflux in unmated gametes is greatly reduced in deflagellated cells, suggesting that much of the Ca movement is associated with the flagellar membrane. Although signaling itself may involve Ca fluxes across the flagellar membrane, it is also possible that a consequence of signaling is release of Ca from intracellular storage sites (perhaps functional equivalents of the sarcoplasmic reticulum). The observed transient increase in Ca efflux rate may reflect a transient increase in the cytoplasmic free-Ca concentration. This increase in cytoplasmic Ca may regulate the later events in mating (such as cell wall release and mating structure activation).

MeSH Terms
Biological Transport, Active Calcium/metabolism Cell Membrane/metabolism Chlamydomonas/physiology Cytoplasm/metabolism Fertilization Flagella/metabolism
Chemicals
Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bloodgood R A
Levin E N
References (56)
56 references, click to expand
  1. Ionic conductances of membranes in ciliated and deciliated Paramecium.
    J Physiol. 1979 Nov;296:49-60 PMID: 529122
  2. Studies on the role of exogenous calcium in fertilization, activation and development of the sea urchin egg.
    Prog Clin Biol Res. 1982;85 Pt B:11-9 PMID: 6812066
  3. The ascidian sperm reaction: Ca2+ uptake in relation to H+ efflux.
    Dev Biol. 1981 Dec;88(2):312-7 PMID: 7308578
  4. Calcium couples flagellar reversal to photostimulation in Chlamydomonas reinhardtii.
    Nature. 1976 Aug 19;262(5570):713-5 PMID: 958445
  5. The ultrastructure of fertilization in Chlamydomonas moewusii.
    Protoplasma. 1975;84(3-4):313-25 PMID: 1178898
  6. Dynamic changes of the egg cortex.
    Dev Biol. 1981 May;84(1):1-26 PMID: 6265303
  7. Free calcium increases explosively in activating medaka eggs.
    Proc Natl Acad Sci U S A. 1977 Feb;74(2):623-7 PMID: 322135
  8. The role of divalent cations in activation of the sea urchin egg. I. Effect of fertilization on divalent cation content.
    J Exp Zool. 1976 Oct;198(1):65-77 PMID: 978163
  9. Reversible inhibition of Chlamydomonas flagellar surface motility.
    J Cell Biol. 1979 Sep;82(3):664-74 PMID: 117013
  10. Aggregation-dependent turnover of flagellar adhesion molecules in Chlamydomonas gametes.
    J Cell Biol. 1980 Jan;84(1):203-10 PMID: 7350168
  11. Initiation of cell wall lysis in gametes of Chlamydomonas reinhardi by isolated flagella of the complementary mating type.
    Exp Cell Res. 1982 Mar;138(1):121-5 PMID: 7067735
  12. Evidence for role of flagella as sensory transducers in mating of Chlamydomonas reinhardi.
    Nature. 1977 Feb 3;265(5593):444-5 PMID: 834294
  13. Uptake of Ca2+ is one of the earliest responses to fertilization of sea urchin eggs.
    J Exp Zool. 1978 Jan;203(1):143-9 PMID: 624920
  14. Membrane-membrane and membrane-ligand interactions in Chlamydomonas mating.
    Soc Gen Physiol Ser. 1980;34:131-52 PMID: 7384832
  15. Gametic differentiation in Chlamydomonas reinhardtii. III. Cell wall lysis and microfilament-associated mating structure activation in wild-type and mutant strains.
    J Cell Biol. 1975 Dec;67(3):623-37 PMID: 1238404
  16. Control of flagellar motion in Chlamydomonas and Euglena by mechanical microinjection of Mg2+ and Ca2+ and by electric current injection.
    J Cell Sci. 1978 Feb;29:233-47 PMID: 415066
  17. Nutritional studies with Chlamydomonas reinhardi.
    Ann N Y Acad Sci. 1953 Oct 14;56(5):831-8 PMID: 13139273
  18. Flagellar membrane agglutination and sexual signaling in the conditional GAM-1 mutant of Chlamydomonas.
    J Cell Biol. 1978 Oct;79(1):74-84 PMID: 701379
  19. Calcium control of waveform in isolated flagellar axonemes of Chlamydomonas.
    J Cell Biol. 1980 Aug;86(2):446-55 PMID: 6447155
  20. Purification of calmodulin from Chlamydomonas: calmodulin occurs in cell bodies and flagella.
    J Cell Biol. 1980 Dec;87(3 Pt 1):764-70 PMID: 6257728
  21. Ca2+ uptake H+ ejection and respiration in sea urchin eggs on fertilization.
    Exp Cell Res. 1970 Nov;63(1):143-6 PMID: 5531477
  22. Artificial deciliation causes loss of calcium-dependent responses in Paramecium.
    Nature. 1976 Nov 11;264(5582):170-2 PMID: 995200
  23. Molecular approaches to the study of fertilization.
    Annu Rev Biochem. 1981;50:815-43 PMID: 6267991
  24. Activation for cell fusion in Chlamydomonas: analysis of wild-type gametes and nonfusing mutants.
    J Cell Biol. 1982 Feb;92(2):378-86 PMID: 7061589
  25. The effect of temperature, Ca2+, Mg2+ and Ni2+ ions on the swimming speed of C. reinhardii determined by quasi-elastic light scattering.
    Exp Cell Res. 1981 Dec;136(2):371-8 PMID: 7308314
  26. Kinetics of adhesion and de-adhesion of Chlamydomonas gametes.
    J Biol Chem. 1979 Nov 10;254(21):10820-9 PMID: 500610
  27. Inhibition of surface capping of macromolecules by local anaesthetics and tranquillisers.
    Nature. 1974 Jul 5;250(461):56-7 PMID: 4841159
  28. Intracellular calcium release at fertilization in the sea urchin egg.
    Dev Biol. 1977 Jul 1;58(1):185-96 PMID: 326602
  29. Isolated flagellar apparatus of Chlamydomonas: characterization of forward swimming and alteration of waveform and reversal of motion by calcium ions in vitro.
    J Cell Sci. 1978 Oct;33:235-53 PMID: 31367
  30. Calcium dependence of the acrosome reaction and activation of guinea pig spermatozoa.
    Exp Cell Res. 1974 Nov;89(1):161-74 PMID: 4435057
  31. A free calcium wave traverses the activating egg of the medaka, Oryzias latipes.
    J Cell Biol. 1978 Feb;76(2):448-66 PMID: 10605450
  32. The role of calcium ions in the acrosome reaction of sea urchin sperm: regulation of exocytosis.
    Exp Cell Res. 1977 Apr;106(1):211-22 PMID: 15851
  33. Participation of calcium in flagellar shortening and regeneration in Chlamydomonas reinhardii.
    Exp Cell Res. 1978 May;113(2):295-301 PMID: 233767
  34. Flagellar elongation and shortening in Chlamydomonas. IV. Effects of flagellar detachment, regeneration, and resorption on the induction of flagellar protein synthesis.
    J Cell Biol. 1978 Jul;78(1):8-27 PMID: 149796
  35. Two distinct mechanisms for redistribution of lymphocyte surface macromolecules. II. Contrasting effects of local anesthetics and a calcium ionophore.
    J Cell Biol. 1978 Nov;79(2 Pt 1):419-26 PMID: 363728
  36. Study of the release of cell wall degrading enzymes during adhesion of Chlamydomonas gametes.
    Exp Cell Res. 1982 Mar;138(1):109-19 PMID: 6802661
  37. Mating in Chlamydomonas: a system for the study of specific cell adhesion. II. A radioactive flagella-binding assay for quantitation of adhesion.
    J Cell Biol. 1976 Jan;68(1):70-9 PMID: 1245546
  38. Intracellular calcium release and the mechanisms of parthenogenetic activation of the sea urchin egg.
    Dev Biol. 1978 Aug;65(2):285-95 PMID: 355009
  39. Experimental dissection of flagellar surface motility in Chlamydomonas.
    J Cell Biol. 1980 Aug;86(2):656-65 PMID: 7400220
  40. Mating in Chlamydomonas eugametos. A scanning electron microscopical study.
    Arch Microbiol. 1976 Aug;109(1-2):31-5 PMID: 962471
  41. Nutritional control of sexuality in Chlamydomonas reinhardi.
    J Gen Physiol. 1954 Jul 20;37(6):729-42 PMID: 13174779
  42. The acrosome reaction of Strongylocentrotus purpuratus sperm. Ion requirements and movements.
    Dev Biol. 1978 Aug;65(2):483-95 PMID: 680373
  43. Chlamydomonas flagella. I. Isolation and electrophoretic analysis of microtubules, matrix, membranes, and mastigonemes.
    J Cell Biol. 1972 Sep;54(3):507-39 PMID: 4558009
  44. Localization of calcium channels in Paramecium caudatum.
    J Physiol. 1977 Sep;271(1):119-33 PMID: 915829
  45. Isolation of protoplasts by means of a "species-specific" autolysine in Chlamydomonas.
    Protoplasma. 1976;88(1):51-64 PMID: 1273306
  46. The effect of phenothiazine and non-phenothiazine inhibitors of calmodulin on platelet calcium fluxes.
    Biochem Biophys Res Commun. 1982 Feb 11;104(3):1066-72 PMID: 7073725
  47. Selective binding of antipsychotics and other psychoactive agents to the calcium-dependent activator of cyclic nucleotide phosphodiesterase.
    J Pharmacol Exp Ther. 1979 Mar;208(3):454-9 PMID: 34709
  48. Calcium displacement by local anesthetics. Dependence on pH and anesthetic charge.
    J Biol Chem. 1979 May 25;254(10):4119-25 PMID: 438180
  49. Sexual agglutinins from the Chlamydomonas flagellar membrane. Partial purification and characterization.
    J Biol Chem. 1982 Apr 25;257(8):4593-602 PMID: 6802837
  50. Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes.
    J Cell Biol. 1980 Mar;84(3):599-617 PMID: 7358792
  51. Selective inhibition of flagellar activity in Chlamydomonas by nickel.
    J Protozool. 1979 May;26(2):235-40 PMID: 114631
  52. The membrane actions of anesthetics and tranquilizers.
    Pharmacol Rev. 1972 Dec;24(4):583-655 PMID: 4565956
  53. Is there a role for the Ca2+ influx during fertilization of the sea urchin egg?
    Dev Biol. 1982 Apr;90(2):284-90 PMID: 7075862
  54. Lidocaine reversibly inhibits fertilization in Chlamydomonas: a possible role for calcium in sexual signalling.
    J Cell Biol. 1982 Sep;94(3):607-12 PMID: 7130274
  55. Can calmodulin inhibitors be used to probe calmodulin effects?
    Biochem Pharmacol. 1981 Jul 15;30(14):2031-2 PMID: 7271894
  56. Calcium influx following fertilization of Urechis caupo eggs.
    Dev Biol. 1977 Jun;57(2):364-74 PMID: 17560
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1983-08-00
Pages
397-404
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2112523
Subset
IM
Grants
NIGMS NIH HHS · GM28766 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com