Comprehensive Physiology Wiley Online Library

Activation of Sperm and Egg During Fertilization

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Chemotaxis (or, the Dating Game)
1.1 Historical Background
1.2 Motility and Chemotactic Substances in Sea Urchin Gametes
1.3 Does Chemotaxis Exist in the Real World?
2 The Acrosome Reaction
2.1 Description of the Phenomenon
2.2 Signal Transduction Molecules
3 Sperm‐Egg Binding
4 Passage of the Sperm Through the Egg Coat
5 Sperm‐Egg Receptors and Speciation
6 A Description of Egg Activation
6.1 What Happens When Sperm Meets Egg?
7 The Role of Calcium in Egg Activation
7.1 Historical Background
7.2 The Natural History of Calcium Changes at Fertilization
7.3 Mechanisms of the Calcium Increase
7.4 How Does the Sperm Trigger the Calcium Increase?
8 What is Calcium Doing to Activate the Egg?
8.1 The Timetable of Fertilization Responses in the Sea Urchin Egg
8.2 Intracellular pH Changes
9 Entry into the Cell Cycle
9.1 Synthesis of Cyclin as a Prerequisite for Mitosis
9.2 Activation of Protein Kinase Activity As a Prerequisite for Mitosis
10 Structural Changes as an Important Concomitant of Fertilization
10.1 Microfilaments
10.2 Microtubules
10.3 Endoplasmic Reticulum
10.4 Introduction of the Centrosome as a Critical Event
10.5 Ooplasmic Segregation
11 Epilogue—Is Fertilization a Unique Event in the Life History of the Organism?
Figure 1. Figure 1.

Diagram of acrosome reaction. Upper part depicts reaction in invertebrate (sea urchin) and lower part comparable reaction in mammal (hamster). In both cases exocytosis of the acrosomal vesicle results in exposure of new surface which will later fuse with egg plasma membrane. In sea urchin case, surface exposed by the acrosome reaction is pushed in front of sperm by polymerization of actin. The new acrosomal process which is formed is also coated with bindin, a protein contained within acrosomal vesicle, which is externalized by acrosomal exocytosis and thence involved in sperm‐egg adhesion.

In mammal (lower part of figure), there is no comparable acrosomal process formed by actin polymerization. Rather, exocytosis exposes surfaces which later fuse with egg surface, although initial fusion is with subacrosomal sperm surfaces which are already exposed before acrosome reaction.

Figure 2. Figure 2.

Cartoon illustrating microscopically visible changes of fertilization in sea urchin. Female pronucleus of unfertilized egg (A) is placed eccentrically in cytoplasm, and prominent feature of egg cortex is presence of numerous cortical granules imbedded in cytoplasm. Sperm‐egg fusion (B) initiates wave of cortical granule exocytosis and elevation of fertilization membrane. Sperm enters through actin‐filled fertilization cone (C). Once inside cytoplasm, sperm centrosome is activated and organizes microtubles around it which are involved in moving sperm and egg pronucleus to egg center (D). Centrosome duplicates and surrounds zygote nucleus (E and F) and then organizes mitotic apparatus (G and H) for first mitosis.

Figure 3. Figure 3.

Illustration of experiment in which current changes and capacitance changes associated with fertilization are simultaneously measured. A depicts experimental setup, in which microelectrode measures voltage around entire egg and patch clamp measures capacitance and ion currents in region of egg where sperm‐egg fusion occurs. Sperm is introduced in pipette, which isolates membrane and allows capacitance measurements to be made in this small area of membrane. As seen in parts B and C, capacitance and ion changes occur simultaneously, indicating that fusion and current changes are temporally associated. Membrane potential change (not shown) also occurs at same time.

Adapted from study of McCulloh and Chambers
Figure 4. Figure 4.

Polyspermy as function of membrane potential in eggs of Urechis caupo. Membrane potential is varied by fertilizing eggs in different concentrations of extracellular sodium (concentration noted in parentheses). As seen, there is increase in number of sperm that can enter egg in relation to degree of depolarization

Adapted from study of Gould‐Somero et al.
Figure 5. Figure 5.

Program of events following fertilization in eggs of sea urchin S. purpuratus at 16° C. The timing is in seconds, presented in a logarithmic fashion on the left‐hand side of the figure. Period of calcium release is highlighted in the period between 30 and 90 s after fertilization.

Figure 6. Figure 6.

Experiment depicting rise in intracellular calcium following fertilization in sea urchin eggs in which various calcium release mechanisms have been prevented. In the IP3 case, IP3‐induced calcium release was prevented by injection of egg with IP3 inhibitor heparin. In cyclic ADP ribose (cADPR) case, cADPR‐induced calcium release was prevented by co‐injection of cADPR analog. As seen, in either case there was release of calcium following fertilization. However, if egg was injected with both inhibitors (lowest tracing), there was no calcium release in response to fertilization

From study of Lee et al.


Figure 1.

Diagram of acrosome reaction. Upper part depicts reaction in invertebrate (sea urchin) and lower part comparable reaction in mammal (hamster). In both cases exocytosis of the acrosomal vesicle results in exposure of new surface which will later fuse with egg plasma membrane. In sea urchin case, surface exposed by the acrosome reaction is pushed in front of sperm by polymerization of actin. The new acrosomal process which is formed is also coated with bindin, a protein contained within acrosomal vesicle, which is externalized by acrosomal exocytosis and thence involved in sperm‐egg adhesion.

In mammal (lower part of figure), there is no comparable acrosomal process formed by actin polymerization. Rather, exocytosis exposes surfaces which later fuse with egg surface, although initial fusion is with subacrosomal sperm surfaces which are already exposed before acrosome reaction.



Figure 2.

Cartoon illustrating microscopically visible changes of fertilization in sea urchin. Female pronucleus of unfertilized egg (A) is placed eccentrically in cytoplasm, and prominent feature of egg cortex is presence of numerous cortical granules imbedded in cytoplasm. Sperm‐egg fusion (B) initiates wave of cortical granule exocytosis and elevation of fertilization membrane. Sperm enters through actin‐filled fertilization cone (C). Once inside cytoplasm, sperm centrosome is activated and organizes microtubles around it which are involved in moving sperm and egg pronucleus to egg center (D). Centrosome duplicates and surrounds zygote nucleus (E and F) and then organizes mitotic apparatus (G and H) for first mitosis.



Figure 3.

Illustration of experiment in which current changes and capacitance changes associated with fertilization are simultaneously measured. A depicts experimental setup, in which microelectrode measures voltage around entire egg and patch clamp measures capacitance and ion currents in region of egg where sperm‐egg fusion occurs. Sperm is introduced in pipette, which isolates membrane and allows capacitance measurements to be made in this small area of membrane. As seen in parts B and C, capacitance and ion changes occur simultaneously, indicating that fusion and current changes are temporally associated. Membrane potential change (not shown) also occurs at same time.

Adapted from study of McCulloh and Chambers


Figure 4.

Polyspermy as function of membrane potential in eggs of Urechis caupo. Membrane potential is varied by fertilizing eggs in different concentrations of extracellular sodium (concentration noted in parentheses). As seen, there is increase in number of sperm that can enter egg in relation to degree of depolarization

Adapted from study of Gould‐Somero et al.


Figure 5.

Program of events following fertilization in eggs of sea urchin S. purpuratus at 16° C. The timing is in seconds, presented in a logarithmic fashion on the left‐hand side of the figure. Period of calcium release is highlighted in the period between 30 and 90 s after fertilization.



Figure 6.

Experiment depicting rise in intracellular calcium following fertilization in sea urchin eggs in which various calcium release mechanisms have been prevented. In the IP3 case, IP3‐induced calcium release was prevented by injection of egg with IP3 inhibitor heparin. In cyclic ADP ribose (cADPR) case, cADPR‐induced calcium release was prevented by co‐injection of cADPR analog. As seen, in either case there was release of calcium following fertilization. However, if egg was injected with both inhibitors (lowest tracing), there was no calcium release in response to fertilization

From study of Lee et al.
References
 1. Abassi, Y. A., and K. R. Foltz. Tyrosine phosphorylation of the egg receptor for sperm at fertilization. Dev. Biol. 164: 430–443, 1994.
 2. Akkaraju, G. R., L. J. Hansen, and R. Jagus. Increase in eukaryotic initiation factor 2B activity following fertilization reflects changes in redox potential. J. Biol. Chem. 266: 24451–24459, 1991.
 3. Alliegro, M. C., and D. R. McClay. Storage and mobilization of extracellular matrix proteins during sea urchin development. Dev. Biol. 125: 208–216, 1988.
 4. Baba, T., S. Azuma, S. Kashiwabara, and Y. Toyoda. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J. Biol. Chem. 269: 31845–31849, 1994.
 5. Baltz, J. M., C. Lechene, and J. D. Biggers. A novel proton permeability dominating intracellular pH in the early mouse embryo. Development 118: 1353–1361, 1993.
 6. Barros, C., C. Capote, C. Perez, J. A. Crosby, M. I. Becker, and A. De Ioannes. Immunodetection of acrosin during the acrosome reaction of harnster guinea‐pig and human spermatozoa. Biol. Res. 25: 31–40, 1992.
 7. Bement, WM. Signal transduction by calcium and protein kinase activation. J. Exp. Zool. 263: 382–397, 1992.
 8. Blackmore, P. F. Rapid non‐genomic actions of progesterone stimulate Ca‐2+ influx and the acrosome reaction in human sperm. Cell. Signal. 5: 531–538, 1993.
 9. Brownlee, C. Tansley Review No. 70. Signal transduction during fertilization in algae and vascular plants. New Phytol. 127: 399–423, 1994.
 10. Byrd, W., and G. Perry. Cytochalasin B blocks sperm incorporation but allows activation of the sea urchin egg. Exp. Cell Res. 126: 333–342, 1980.
 11. Cameron, L. A. and D. L. Poccia. In vitro development of the sea urchin male pronucleus. Dev. Biol. 162: 568–578, 1994.
 12. Cameron, R. A., J. E. Minor, D. Nishioka, R. J. Britten, and E. H. Davidson. Locale and level of bindin mRNA in maturing testis of the sea urchin, Strongylocentrotus purpuratus. Dev. Biol. 142: 44–49, 1990.
 13. Carron, C. P., and F. J. Longo. Relation of cytoplasmic alkalinization to microvillar elongation and microfilament formation in the sea urchin egg. Dev. Biol. 89: 128–137, 1982.
 14. Chambers, E. L. Na is essential for activation of the inseminated sea urchin egg. J. Exp. Zool. 197: 149–154, 1976.
 15. Chambers, E. L., B. C. Pressman, and R. E. Rose. The activation of sea urchin eggs by the divalent ionophores A23187 and X‐537A. Biochem. Biophys. Res. Commun. 60: 126–132, 1974.
 16. Chinkers, M., and D. L. Garbers. Signal transduction by guanylyl cyclases. Annu. Rev. Biochem. 60: 553–576, 1991.
 17. Ciapa, B., B. Borg, and M. Whitaker. Polyphosphoinositide metabolism during the fertilization wave in sea urchin eggs. Development 115: 187–195, 1992.
 18. Ciapa, B., and D. Epel. A rapid change in phosphorylation on tyrosine accompanies fertilization of sea urchin eggs. FEBS Lett. 295: 167–170, 1991.
 19. Clapper, D. L., and D. Epel. Sperm motility in the horseshoe crab. III. Isolation and characterization of a sperm motility initiating peptide. Gamete Res. 6: 315–326, 1982.
 20. Clapper D. L., T. F. Walseth, P. J. Dargie, and H. C. Lee. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J. Biol. Chem. 262: 9561–9568, 1987.
 21. Collins, F. D. A reevaluation of the fertilizin hypothesis of sperm agglutination and the description of a novel form of sperm adhesion. Dev. Biol. 49: 381–394, 1976.
 22. Collins, F. D., and D. Epel. The role of calcium ions in the acrosome reaction of sea urchin sperm: regulation of exocytosis. Exp. Cell Res. 106: 211–222, 1977.
 23. Cook, S. P., and D. F. Babcock. Selective modulation by cGMP of the K+ channel activated by speract. J. Biol. Chem. 268: 22402–22407, 1993.
 24. Cook, S. P., C. J. Brokaw, C. H. Muller, and D. F. Babcock. Sperm chemotaxis: egg peptides control cytosolic calcium to regulate flagellar responses. Dev. Biol. 165: 10–19, 1994.
 25. Cuthbertson, K. S., D. G. Whittingham, and P. H. Cobbold. Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature 294: 754–757, 1981.
 26. Dangott, L. J., and D. L. Garbers. Identification and partial characterization of the receptor for speract. J. Biol. Chem. 259: 13712–13716, 1984.
 27. Darszon, A., P. Labarca, C. Beltran, J. Garcia‐Soto, and A. Lievano. Sea urchin sperm: an ion channel reconstitution study case. Methods (Orlando) 6: 37–50, 1994.
 28. Davidson, E. H. Gene activity in early development (3rd ed.). Orlando: Academic Press, 1986.
 29. Denny, M. W., and M. F. Shibata. Consequences of surf‐zone turbulence for settlement and external fertilization. Am. Nat. 134: 859–889, 1989.
 30. Dholakia, J. N., and J. A. Wahba. Phosphorylation of the guanine nucleotide exchange factor from rabbit reticulocytes regulates its activity in polypeptide chain initiation. Proc. Natl. Acad. Sci. U.S.A. 85: 51–54, 1988.
 31. Dholakia, J. N., Xu, M. B. Hille, and A. J. Wahba. Purification and characterization of sea urchin initiation factor 2: the requirement of guanine nucleotide exchange factor for the release of eukaryotic polypeptide chain initiation factor 2‐bound GDP. J. Biol. Chem. 265: 19319–19323, 1990.
 32. Dube, F., and D. Epel. The relation between intracellular pH and rate of protein synthesis in sea urchin eggs and the existence of a pH‐independent event triggered by ammonia. Exp. Cell Res. 162: 191–204, 1986.
 33. Dube, F., T. Schmidt, C. H. Johnson, and D. Epel. The hierarchy of requirements for an elevated intracellular pH during early development of sea urchin embryos. Cell 40: 657–666, 1985.
 34. Eisenbach, M., and D. Ralt. Precontact mammalian sperm‐egg communication and role in fertilization. Am. J. Physiol. 262 (Cell Physiol. 31): C1095–C1101, 1992.
 35. Epel, D. A primary metabolic change of fertilization: interconversion of pyridine nucleotides. Biochem. Biophys. Res. Commun. 17: 62–68, 1964.
 36. Epel, D. Protein synthesis in sea urchin eggs: a ‘late’ response to fertilization. Proc. Natl. Acad. Sci. U.S.A. 57: 899–906, 1967.
 37. Epel, D. Activation of an Na +‐dependent amino acid transport system upon fertilization of sea urchin eggs. Exp. Cell Res. 72: 74–89, 1972.
 38. Epel, D., Na + ‐H+ exchange and fertilization. In: Na+ ‐H+ Exchange, edited by S. Grinstein. Boca Raton, FL: CRC Press, 1988, p. 209–226.
 39. Epel, D. The initiation of development at fertilization. Cell Diff. Dev. 29: 1–13, 1990.
 40. Epel, D., N. S. Cross, and N. Epel. Flagellar motility is not involved in the incorporation of the sperm into the egg at fertilization. Dev. Growth Diff. 19: 15–21, 1977.
 41. Epel, D., C. Patton, R. W. Wallace, and W. Y. Cheung. Calmodulin activates NAD kinase of sea urchin eggs: an early event of fertilization. Cell 23: 543–549, 1981.
 42. Epel, D., R. Steinhardt, T. Humphreys, and D. Mazia. An analysis of the partial metabolic derepression of sea urchin eggs by ammonia. The existence of independent pathways. Dev. Biol. 40: 245–255, 1974.
 43. Fields, S. Pheromone response in yeast. Trends Biochem. Sci. 15: 270–273, 1990.
 44. Fisher, G. W., and L. I. Rebhun. Sea urchin egg cortical granule exocytosis is followed by a burst of membrane retrieval via uptake into coated vesicles. Dev. Biol. 99: 456–472, 1983.
 45. Foerder, C. A., and B. M. Shapiro. Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. Proc. Natl. Acad. Sci. U.S.A. 75: 3183–3187, 1977.
 46. Foltz, K. R. The sea urchin egg receptor for sperm. Semin. Dev. Biol. 5: 243–253, 1994.
 47. Foltz, K. R., J. S. Partin and W. J. Lennarz. Sea urchin egg receptor for sperm: sequence similarity of binding domain and hsp70. Science 259: 1421–1425, 1993.
 48. Galione, A., H. C. Lee, and W. B. Busa. Calcium‐induced calcium release in sea urchin egg homogenates: modulation by cyclic ADP‐ribose. Science 253: 1143–1146, 1991.
 49. Galione, A., A. Mcdougall, W. B. Busa, N. Willmott, I. Gillot, and M. Whitaker. Redundant mechanisms of calcium‐induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science 261: 348–352, 1993.
 50. Galione, A., A. White, N. Willmott, M. Turner, B.V.L. Potter, and S. P. Watson. cGMP mobilizes intracellular calcium. Nature 365: 456–459, 1993.
 51. Garbers, D. L. Molecular basis of fertilization. Annu. Rev. Biochem. 58: 719–742, 1989.
 52. Gerhart, J., and R. Keller. Region‐specific cell activities in amphibian gastrulation. Annu. Rev. Cell Biol. 2: 201–292, 1986.
 53. Gilkey, J. C., L. F. Jaffe, E. B. Ridgeway, and G. T. Reynolds. A free calcium wave traverses the activating egg of the Medaka, Oryzias latipes. J. Cell Biol. 76: 448–466, 1978.
 54. Gillot, I., and M. Whitaker. Imaging calcium waves in eggs and embryos. J. Exp. Biol. 184: 213–219, 1993.
 55. Goodenough, U. W., E V. Armbrust, A. M. Campbell, P. J. Ferris, and R. L. Jones. Molecular genetics of sexuality in Chlamydomonas. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 21–44, 1995.
 56. Gould, M., and J. L. Stephano. Electrical responses of eggs to acrosomal protein similar to those induced by sperm. Science 235: 1654–1656, 1987.
 57. Gould, M. C., and J. L. Stephano. Peptides from sperm acrosomal protein that initiate egg development. Dev. Biol. 146: 509–518, 1991.
 58. Gould, M. C., and J. L. Stephano. Nuclear and cytoplasmic pH increase at fertilization in Urechis caupo. Dev. Biol. 159: 608–617, 1993.
 59. Gould‐Somero, M., L. A. Jaffe, and L. Z. Holland. Electrically‐mediated fast polyspermy block in eggs of the marine worm Urechis caupo. J. Cell. Biol. 82: 426–440, 1979.
 60. Grainger, J. L. The unmasking of maternal mRNA during oocyte maturation and fertilization. Genet. Eng. NY 16: 229–239, 1994.
 61. Grainger, J. L., V. M. Trumpbour, and A. C. Corbett. Mechanism of activation of sea urchin egg messenger rnps. J. Cell Biol. III (2): 369A, 1990.
 62. Grainger, J. L., and M. M. Winkler. Fertilization triggers unmasking of maternal messenger RNAs in sea urchin eggs. Mol. Cell. Biol. 7: 3947–3954, 1987.
 63. Haino‐Fukushima, K. Studies on the egg‐membrane lysin of Tegula pfeifferi. The reaction mechanism of the egg‐membrane lysin. Biochim. Biophys. Acta. 352: 179–191, 1974.
 64. Hamaguchi, Y., and Y. Hiramoto. Activation of sea urchin eggs by microinjection of calcium buffers. Exp. Cell Res. 134: 171–179, 1981.
 65. Hamill, D., J. Davis, J. Drawbridge, and K. A. Suprenant. Polyribosome targeting to microtubules: enrichment of specific mRNAs in a reconstituted microtubule preparation from sea urchin embryos. J. Cell Biol. 127: 973–984, 1994.
 66. Heilbrunn, L. V. An Outline of General Physiology. Philadelphia: Saunders, 1937.
 67. Heinecke, J. W., K. E. Meier, J. A. Lorenzen, and B. M. Shapiro. A specific requirement for protein kinase C in activation of the respiratory burst oxidase of fertilization. J. Biol. Chem. 265: 7717–7720, 1990.
 68. Henson, J. H., D. A. Begg, S. M. Beaulieu, D. J. Fishkind, E. M. Bonder, M. Teraski, and M. Lebeche. A calsequestrinlike protein in the endoplasmic reticulum of the sea urchin: localization and dynamics in the egg and first cell cycle embryo. J. Cell Biol. 109: 149–162, 1989.
 69. Hille, M. B., J. N. Dholakia, A. Wahba, E. Fanning, L. Stimler, Z. Xu, and Z. Yablonka‐Reuveni. In‐vivo and in‐vitro evidence supporting co‐regulation of translation in sea‐urchin eggs by polypeptide initiation factors, pH optimization, and mRNAs. J. Reprod. Fertil. Suppl. 42: 235–248, 1990.
 70. Hinegardner, R. T., B. Rao, and D. E. Feldman. The DNA synthetic period during early development of the sea urchin egg. Exp. Cell Res. 36: 53–59, 1964.
 71. Hofmann, A., and C. Glabe. Bindin, a multifunctional sperm ligand and the evolution of new species. Semin. Dev. Biol. 5: 233–242, 1994.
 72. Hoshi, M. Lysins. In: Biology of Fertilization, edited by C. B. Metz, and A. Monroy. San Diego: Academic Press, 1985, vol. 2, p. 431–462.
 73. Hoshi, M., T. Nishigaki, A. Ushiyama, T. Okinaga, K. Chiba, and M. Matsumoto. Egg‐jelly signal molecules for triggering the acrosome reaction in starfish spermatozoa. Int. J. Dev. Biol. 38: 167–174, 1994.
 74. Hoshi, M., T. Okinaga, K. Kontani, T. Araki, and K. Chiba. Acrosome reaction‐inducing glycoconjugates in the jelly coat of starfish eggs. In: Comparative Spermatology: 20 Years After, edited by B. Baccetti. New York: Raven Press, 1991, p. 175–183.
 75. Hunt, T., P. Herbert E. A. Campbell, C. Delidakis, and R. J. Jackson. The use of affinity chromatography on 2′5′ ADP‐sepharose reveals a requirement for NADPH, thioredoxin and thioredoxin reductase for the maintenance of high protein synthesis activity in rabbit reticulocyte lysates. Eur. J. Biochem. 131: 303–311, 1983.
 76. Ii, I., and L. I. Rebhun. Acid release following activation of surf clam (Spisula solidissima) eggs. Dev. Biol. 72: 195–200, 1979.
 77. Isono, N. Carbohydrate metabolism in sea urchin eggs. J. Fac. Sci. Univ. Tokyo 10: 37–53, 1963.
 78. Iwasa, K. H., G. Ehrenstein, L. J. DeFelice, and J. T. Russell. High concentration of inositol 1,4,5‐triphosphate in sea urchin sperm. Biochem. Biophys. Res. Commun. 172: 932–938, 1990.
 79. Jaffe, L. A. Fast block to polyspermy in sea urchin eggs is electrically mediated. Nature 261: 68–71, 1976.
 80. Jaffe, L. A., N. L. Cross, and B. Picheral. Studies of the voltage‐dependent polyspermy block using cross‐species fertilization of amphibians. Dev. Biol. 98: 319–326, 1983.
 81. Jaffe, L. A., and M. Gould. Polyspermy preventing mechanisms. In: Biology of Fertilization, edited by C. B. Metz, and A. Monroy. San Diego: Academic Press, 1985, vol. 3, p. 223–251.
 82. Jaffe, L. A., M. Gould‐Somero, and L. Holland. Studies of the mechanisms of the electrical poslyspermy block using cross‐species fertilization. J. Cell Biol. 92: 616–621, 1982.
 83. Jaffe, L. A., and K. R. Robinson. Membrane potential of the unfertilized sea urchin egg. Dev. Biol. 62: 215–282, 1978.
 84. Jaffe, L. A., M. Terasaki. Structural changes of the endoplasmic reticulum of sea urchin eggs during fertilization. Dev. Biol. 156: 566–573, 1993.
 85. Jaffe, L. A., and L. G. Tilney. Actin, microvilli, and the fertilization cone of sea urchin eggs. J. Cell Biol. 87: 771–782, 1980.
 86. Jaffe, L. F., The role of calcium explosions, waves and pulses in activating eggs. In Biology of Fertilization, edited by C. B. Metz and A. Monroy. San Diego: Academic Press, 1985, vol. 3, p. 127–165.
 87. Jaffe, L. F., The roles of intermembrane calcium in polarizing and activating eggs. In: Mechanisms of Fertilization: Plants to Humans, edited by B. Dale. Berlin: Springer‐Verlag, 1990, p. 389–418.
 88. Jeffery, W. R., and B. J. Swalla. The myoplasm of ascidian eggs: a localized cytoskeletal domain with multiple roles in embryonic development. Semin. Cell Biol. 1: 373–381, 1990.
 89. Jiang, W. P., P. A. Veno, R. W. Wood, G. Peaucellier, and W. H. Kinsey. pH regulation of an egg cortex tyrosine kinase. Dev. Biol. 146: 81–88, 1991.
 90. Johnson, C. H., and D. Epel. Starfish oocyte maturation and fertilization: intracellular pH is not involved in activation. Dev. Biol. 92: 461–469, 1982.
 91. Johnson, J. D., D. Epel, and M. Paul. Na+‐H+ exchange is required for activation of sea urchin eggs after fertilization. Nature 262: 661–664, 1976.
 92. Johnston, R. N., and M. Paul. Calcium influx following fertilization of Urechis caupo eggs. Dev. Biol. 57: 364–374, 1977.
 93. Kay, E. S., and B. M. Shapiro. The formation of the fertilization membrane of the sea urchin egg. In Biology of Fertilization, edited by C. B. Metz and A. Monroy. San Diego: Academic Press, 1985, vol. 3, p. 45–81.
 94. Keller, S. H., and V. D. Vacquier. The isolation of acrosome‐reaction‐inducing glycoproteins from sea urchin egg jelly. Dev. Biol. 162: 304–312, 1994.
 95. Kellogg, D. R., M. Moritz, and B. M. Alberts. The centrosome and cellular organization. Annu. Rev. Biochem. 63: 639–674, 1994.
 96. Kelso‐Winemiller, L. C., and M. M. Winkler. Unmasking of stored maternal messenger RNAs and the activation of protein synthesis at fertilization in sea urchins. Development 111: 623–634, 1991.
 97. Kline, D., L. Simoncini, G. Mandel, R A. Maue, R. T. Kado, and L. A. Jaffe. Fertilization events induced by neurotransmitters after injection of messenger RNA in Xenopus eggs. Science 241: 464–467, 1988.
 98. Lee, H. C., and R. Aarhus. A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP‐ribose. J. Biol. Chem. 270: 2152–2157, 1995.
 99. Lee, H. C., R. Aarhus, and R. M. Graeff. Sensitization of calcium‐induced calcium release by cyclic ADP‐ribose and calmodulin. J. Biol. Chem. 270: 9060–9066, 1995.
 100. Lee, H. C., R. Aarhus, and T. F. Walseth. Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261: 352–355, 1993.
 101. Lee, H. C., and D. L. Garbers. Modulation of the voltage‐sensitive Na + /H + exchange in sea urchin. J. Biol. Chem. 261: 16026–16032, 1986.
 102. Lee, H. C., A. Galione, and T. F. Walseth. Cyclic ADP‐ribose: metabolism and calcium mobilizing function. Vitam. Horm. 48: 199–257, 1994.
 103. Lee, H. C., C. Johnson, and D. Epel. Changes in internal pH associated with initiation of motility and acrosome reaction of sea urchin sperm. Dev. Biol. 95: 31–45, 1983.
 104. Lee, Y.‐H., T. Ota, and V. D. Vacquier. Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol. Biol. Evol. 12: 231–238, 1995.
 105. Lennarz, W. J. Fertilization in sea urchins: how many different molecules are involved in gamete interaction and fusion? Zygote 2: 1–4, 1994.
 106. Longo, F. J., S. Cook, D. H. McCulloch, P. I. Ivonnet, and E. L. Chambers. Stage leading to and following fusion of sperm and egg plasma membranes. Zygote 2: 317–331, 1994.
 107. Lopez, A., S. J. Miraglia, and C. G. Glabe. Structure/function analysis of the sea urchin sperm adhesive protein bindin. Dev. Biol. 156: 24–33, 1993.
 108. Lynn, J. W., D. H. Mcculloh, and E. L. Chambers. Voltage clamp studies of fertilization in sea urchin eggs: II. Current patterns in relation to sperm entry, nonentry, and activation. Dev. Biol. 128: 305–323, 1988.
 109. Maruta, H., Chemotaxis during the development of cellular slime molds. In: Biology of Fertilization, edited by C. B. Metz, and A. Monroy. San Diego: Academic Press, 1985, vol. 2, p. 255–276.
 110. Mazia, D. The release of calcium in Arbacia eggs upon fertilization. J. Cell Comp. Physiol. 10: 291–304, 1935.
 111. Mazia, D. Chromosome cycles turned on in unfertilized sea urchin eggs exposed to NH4OH. Proc. Natl. Acad. Sci. U.S.A. 71: 690–693, 1974.
 112. Mazia, D. The chromosome cycle and the centrosome cycle in the mitotic cycle. Int. Rev. Cytol. 100: 49–92, 1987.
 113. Mcculloh, D., and E. L. Chambers. Fusion of membranes during fertilization: increases of the sea urchin egg's membrane capacitance and membrane conductance at the site of contact with the sperm. J. Gen. Physiol. 99: 137–175, 1992.
 114. Mcpherson, S. M., P. S. Mcpherson, L. Mathews, K. P. Campbell, and F. J. Longo. Cortical localization of a calcium release channel in sea urchin eggs. J. Cell Biol. 116: 1111–1121, 1992.
 115. Mead, K. S., and D. Epel. Beakers versus breakers: how fertilization in the laboratory differs from fertilization in nature. Zygote 3: 95–99, 1995.
 116. Miller, R. L., Sperm chemo‐orientation in the metazoa. In: Biology of Fertilization, edited by C. B. Metz, and A. Monroy. San Diego: Academic Press, 1985, vol. 2, p. 276–340.
 117. Minor, J. E., D. R. Fromson, R. J. Britten, and E. H. Davidson. Comparison of the bindin proteins of Strongylocentrotus franciscanus, Strongylocentrotus purpuratus, and Lytechinus variegatus: sequences involved in the species specificity of fertilization. Mol. Biol. Evol. 8: 781–795, 1991.
 118. Moore, K. L., and W. H. Kinsey. Identification of an abl‐related protein tyrosine kinase in the cortex of the sea urchin egg: possible role at fertilization. Dev. Biol. 164: 444–455, 1994.
 119. Nielsen, O., and J. Davey. Pheromone communication in the fission yeast Schizosaccharomyces pombe. Semin. Cell Biol. 6: 95–104, 1995.
 120. Nishioka, D., R. D. Ward, D. Poccia, C. Kostacos, and J. E. Minor. Localization of bindin expression during sea urchin spermatogenesis. Mol. Reprod. Dev. 27: 181–190, 1990.
 121. Oberdorf, J., C. Vilar, and D. Epel. The localization of PI and PIP kinase in the sea urchin egg and their modulation following fertilization. Dev. Biol. 131: 236–243, 1989.
 122. Oberdorf, J. A., J. F. Head, and B. Kaminer. Calcium uptake and release by isolated cortices and microsomes from the unfertilized egg of the sea urchin Strongylocentrotus droebachiensis. J. Cell Biol. 102: 2205–2210, 1986.
 123. Oberdorf, J. A., D. Lebeche, J. F. Head, and B. Kaminer. Identification of a calsequestrin‐like protein from sea urchin eggs. J. Biol. Chem. 263: 6806–6809, 1988.
 124. Ohlendieck, K., J. S. Partin, R. L. Stears, and W. J. Lennarz. Developmental expression of the sea urchin egg receptor for sperm. Dev. Biol. 165: 53–62, 1994.
 125. Paul, M., and D. Epel. Fertilization‐associated light scattering changes in eggs of the sea urchin, Strongylocentrotus purpuratus. Exp. Cell Res. 65: 281–288, 1971.
 126. Paweletz, N., D. Mazia, and E. ‐M. Finze. Fine structural studies of the bipolarization of the mitotic apparatus in the fertilized sea urchin egg: I. The structure and behavior of centrosomes before fusion of the pronuclei. Eur. J. Cell Biol. 44: 195–204, 1987.
 127. Peaucellier, G. Acid release at meiotic maturation of oocytes in the polychaete annelid Sabellaria alveolata. Experientia 34: 789–90, 1978.
 128. Pillai, M. C., T. S. Shields, R. Yanagimachi, and G. N. Cherr. Isolation and partial characterization of the sperm motility initiation factor from eggs of the Pacific herring, Clupea pallasi. J. Exp. Zool. 265: 336–342, 1993.
 129. Pines, J. Cyclins and cyclin‐dependent kinases: a biochemical view. Biochem. J. 308: 697–711, 1995.
 130. Poenie, M., and D. Epel. Ultrastructural localization of intracellular calcium stores by a new cytochemical method. J. Hist. Cytochem. 35: 939–956, 1987.
 131. Preuss, D. Being fruitful: genetics of reproduction in Arabidopsis. Trends Genet. 11: 147–153, 1995.
 132. Rakow, T. L., and S. S. Shen. Multiple stores of calcium are released in the sea urchin egg during fertilization. Proc. Natl. Acad. Sci. U.S.A. 87: 9285–9289, 1990.
 133. Ralt, D., M. Goldenberg, P. Fetterolf, D. Thompson, J. Dor, S. Mashiach, D. L. Garbers, and M. Eisenbach. Sperm attraction to a follicular factor(s) correlates with human egg fertilizability. Proc. Natl. Acad. Sci. U.S.A. 88: 2840–2844, 1991.
 134. Rees, B. B., C. Patton, J. L. Grainger, and D. Epel. Protein synthesis increases after fertilization of sea urchin eggs in the absence of an increase in intracellular pH. Dev. Biol. 169: 683–698, 1995.
 135. Ridgway, E. B., J. C. Gilkey, and L. F. Jafe. Free calcium increases explosively in activating medaka eggs. Proc. Natl. Acad. Sci. U.S.A. 74: 623–627, 1977.
 136. Ruderman, J., F. Luca, E. Shibuya, K. Gavin, T. Boulton, and M. Cobb. Control of the cell cycle in early embryos. Cold Spring Harb. Symp. Quant. Biol. vol. Lvi. The Cell Cycle, p. 495–502, 1991.
 137. Schackmann, R. W., R. Christen, and B. M. Shapiro. Membrane potential depolarization and increased intracellular pH accompany the acrosome reaction of sea urchin sperm. Proc. Natl. Acad. Sci. U.S.A. 78: 6066–6070, 1981.
 138. Schatten, G. Motility during fertilization. Int. Rev. Cytol. 79: 59–163, 1982.
 139. Schatten, G. The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev. Biol. 165: 299–335, 1994.
 140. Schatten, G., T. Bestor, R. Balczon, J. Henson, and H. Schatten. Intracellular pH shift leads to microtubule assembly and microtubule‐mediated motility during sea urchin fertilization: correlations between elevated intracellular pH and microtubule activity and depressed intracellular pH and microtubule disassembly. Eur. J. Cell Biol. 36: 116–127, 1985.
 141. Schatten, G., and H. Schatten. Fertilization: motility, the cytoskeleton and the nuclear architecture. Oxf. Rev. Reprod. Biol. 9: 322–378, 1987.
 142. Schmidt, T., and D. Epel. High hydrostatic pressure and the dissection of fertilization responses I. The relationship between cortical granule exocytosis and proton efflux during fertilization of the sea urchin egg. Exp. Cell Res. 146: 235–248, 1983.
 143. Schmidt, R., C. Patton, and D. Epel. Is there a role for the Ca2+ influx during fertilization of the sea urchin egg? Dev. Biol. 90: 284–290, 1982.
 144. Schomer, B., 1995 (unpublished results).
 145. Schroeder, T. E. Surface area change at fertilization: resorption of the mosaic membrane. Dev. Biol. 70: 306–326, 1979.
 146. Shakes, D. C., and S. Ward. Mutations that disrupt the morphogenesis and localization of a sperm‐specific organelle in Caenorhabditis elegans. Dev. Biol. 134: 307–316, 1989.
 147. Shapiro, B. M. The control of oxidant stress at fertilization. Science 252: 533–536, 1991.
 148. Shaw, A., D. E. McRee, V. D. Vacquier, and C. D. Stout. The crystal structure of lysin, a fertilization protein. Science 262: 1864–1867, 1993.
 149. Sheets, M. D., C. A. Fox, T. Hunt, G. Vande Woude, and M. Wickens. The 3′‐untranslated regions of c‐mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 8: 926–938, 1994.
 150. Shen, S. S. Na+‐H+ antiport during fertilization of the sea urchin egg is blocked by W‐7 but is insensitive to K252a and H‐7. Biochem. Biophys. Res. Commun 161: 1100–1108, 1989.
 151. Shen, S. S., and R. A. Steinhardt. Direct measurement of intracellular pH during metabolic derepression of the sea urchin egg. Nature 272: 253–254, 1978.
 152. Shen, S. S., and R. A. Steinhardt. Time and voltage windows for reversing the electrical block to fertilization. Proc. Natl. Acad. Sci. U.S.A. 81: 1436–1439, 1984.
 153. Shibuya, E. K., A. J. Polverino, E. Chang, M. Wigler, and J. V. Ruderman. V. Oncogenic Ras triggers the activation of 42‐kDa mitogen‐activated protein kinase in extracts of quiescent Xenopus oocytes. Proc. Natl. Acad. Sci. U.S.A. 89: 9831–9835, 1992.
 154. Shilling, F., G. Mandel, and L. A. Jaffe. Activation by serotonin of starfish eggs expressing the rat serotonin 1c receptor. Cell Regul. 1: 465–470, 1990.
 155. Simon, R., J. P. Tassan, and J. D. Richter. Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev. 6: 2580–2591, 1992.
 156. Singh, S., D. G. Lowe, D. S. Thorpe, H. Rodriguez, W.‐J. Kuang, L. J. Dangott, M. Chinkers, D. V. Goeddel, and D. L. Garbers. Membrane guanylate cyclase is a cell‐surface receptor with homology to protein kinases. Nature 334: 708–712, 1988.
 157. Speksnijder, J., D. W. Corson, C. Sardet, and L. F. Jaffe. Free calcium pulses following fertilization in the ascidian egg. Dev. Biol. 135: 182–190, 1989.
 158. Speksnijder, J., C. Sardet, and L. F. Jaffe. The activation wave of calcium in the ascidian egg and its role in ooplasmic segregation. J. Cell Biol. 110: 1589–1598, 1990.
 159. Spudich, A., Actin organization in the sea urchin egg cortex. In: Current Topics in Developmental Biology, Cytoskeleton in Development, edited by E. L. Bearer. San Diego, CA: Academic Press, 1992, vol. 26, p. 9–21.
 160. Steinhardt, R. A., and D. Epel. Activation of sea urchin eggs by a calcium ionophore. Proc. Natl. Acad. Sci. U.S.A. 71: 1915–1919, 1974.
 161. Steinhardt, R., R. Zucker, and G. Schatten. Intracellular calcium release at fertilization in the sea urchin egg. Dev. Biol. 58: 185–196, 1977.
 162. Suprenant, K. A. Alkaline pH favors microtubule self‐assembly in surf clam, Spisula solidissima, oocyte extracts. Exp. Cell Res. 184: 167–180, 1989.
 163. Suzuki, N. Structure and function of sea urchin egg jelly molecules. Zool. Sci. (Tokyo) 7: 355–370, 1990.
 164. Suzuki, N. Structure, function and biosynthesis of sperm‐activating peptides and fucose sulfate glycoconjugate in the extracellular coat of sea urchin eggs. Zool. Sci. (Tokyo) 12: 13–27, 1995.
 165. Swalla, B, and W. R. Jeffery. A maternal RNA localized in the yellow crescent is segregated to the larval muscle cells during ascidian development. Dev. Biol. 170: 353–364, 1995.
 166. Swann, K. How does a spermatozoon activate an oocyte?: The soluble sperm oscillogen hypothesis. Zygote 1: 273–276, 1993.
 167. Swann, K. Ca‐2+ oscillations and sensitization of Ca‐2 + release in unfertilized mouse eggs injected with a sperm factor. Cell Calcium 15: 331–339, 1994.
 168. Swann, K., and J.‐P. Ozil. Dynamics of the calcium signal that triggers mammalian egg activation. Int. Rev. Cytol. 152: 183–222, 1994.
 169. Swann, K., and M. Whitaker. Stimulation of the Na/H exchanger of sea urchin eggs by phorbol ester. Nature 314: 274–277, 1985.
 170. Swann, K., and M. Whitaker. The part played by inositol trisphosphate and calcium in the propagation of the fertilization wave in sea urchin eggs. J. Cell Biol. 103: 2333–2342, 1986.
 171. Swanson, W., and V. D. Vacquier. Extraordinary divergence and positive Darwinian selection in a fusogenic protein coating the acrosomal process of abalone spermatozoa. Proc. Natl. Acad. Sci. U.S.A. 92: 4957–4961, 1995.
 172. Swezey, R. R., and D. Epel. Regulation of glucose‐6‐phosphate dehydrogenase activity in sea urchin eggs by reversible association with cell structural elements. J. Cell. Biol. 103: 1509–1515, 1986.
 173. Swezey, R. R., and D. Epel. Enzyme stimulation upon fertilization is revealed in electrically permeabilized sea urchin eggs. Proc. Natl. Acad. Sci. U.S.A. 85: 812–816, 1988.
 174. Swezey, R. R., and D. Epel. The in vivo rate of glucose‐6‐phosphate dehydrogenase activity in sea urchin eggs determined with a photolabile substrate. Dev. Biol. 169: 733–744, 1995.
 175. Terasaki, M., and L. A. Jaffe. Organization of the sea urchin egg reorganization at fertilization. J. Cell Biol. 114: 929–940, 1991.
 176. Tian, W.‐N., J. N. Pignatare, and R. C. Stanton. Signal transduction proteins that associate with the platelet‐derived growth factor (PDGF) receptor mediate the PDGF‐induced release of glucose‐6‐phosphate dehydrogenase from permeabilized cells. J. Biol. Chem. 269: 14798–14805, 1994.
 177. Tilney, L., The acrosomal reaction. In: Biology of Fertilization, edited by C. B. Metz, and A. Monroy. San Diego: Academic Press, 1985, vol. 2, p. 157–215.
 178. Tyler, A., and B. S. Tyler. Physiology of fertilization and early development. In: Physiology of Echinodermata edited by R. Boolootian. New York: Interscience 1966, p. 683–741.
 179. Vacquier, V. D. Dynamic changes of the egg cortex. Dev. Biol. 84: 1–26, 1981.
 180. Vacquier, V. D., K. R. Carner, and C. D. Stout. Species‐specific sequences of abalone lysin, the sperm protein that creates a hole in the egg envelope. Proc. Natl. Acad. Sci. U.S.A. 87: 5792–5796, 1990.
 181. Vacquier, V. D., and Y.‐H. Lee. Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein. Zygote 1: 181–196, 1993.
 182. Vacquier, V. D., and J. E. Payne. Methods for quantitating sea urchin sperm‐egg binding. Exp. Cell Res. 82: 227–235, 1973.
 183. Vacquier, V. D., W. J. Swanson, and M. E. Hellberg. What have we learned about sea urchin sperm binding? Dev. Growth Diff. 37: 1–10, 1995.
 184. Ward, C. R., and G. S. Kopf. Molecular events mediating sperm activation. Dev. Biol. 158: 9–34, 1993.
 185. Ward, G. E., C. J. Brokaw, D. L. Garbers, and V. D. Vacquier. Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from the egg jelly layer. J. Cell. Biol. 101: 2324–2329, 1985.
 186. Ward, G. E., G. W. Moy, and V. D. Vacquier. Dephosphorylation of sea urchin sperm guanylate cyclase during fertilization. Adv. Exp. Med. Biol. 207: 359–382, 1986.
 187. Webb, D. J., and R. Nuccitelli. Direct measurement of intracellular pH changes in Xenopus eggs at fertilization and cleavage. J. Cell Biol. 91: 562–567, 1981.
 188. Whalley, T., A. McDougall, I. Crossley, K. Swann, and M. Whitaker. Internal calcium release and activation of sea urchin eggs by cGMP are independent of the phosphoinositide signaling pathway. Mol. Biol. Cell 3: 373–383, 1992.
 189. Whitaker, M. Exocytosis in sea urchin eggs. Ann. NY Acad. Sci. 710: 248–253, 1994.
 190. Whitaker, M., and M. Aitchison. Calcium‐dependent polyphosphoinositide hydrolysis is associated with exocytosis in vitro. FEBS. Lett. 182: 119–124, 1985.
 191. Whitaker, M., and R. Patel. Calcium and cell cycle control. Development 108: 525–542, 1990.
 192. Whitaker, M. J., and R. A. Steinhardt. The relation between the increase in reduced nicotinamide nucleotides and the initiation of DNA synthesis in sea urchin eggs. Cell 25: 95–103, 1981.
 193. Whitaker, M. J., and R. A. Steinhardt. Ionic signalling in the sea urchin egg at fertilization. In: Biology of Fertilization, edited by C. B. Metz, and A. Monroy. San Diego: Academic Press, 1985, vol. 3, p. 168–222.
 194. Whitaker, M., and K. Swann. Lighting the fuse at fertilization. Development. 117: 1–12, 1993.
 195. Whitaker, M., K. Swann, and I. Crossley. What happens during the latent period at fertilization? In: Mechanisms of Egg Activation, edited by R. Nuccitelli, G. N. Cherr, and W. H. Clark, Jr. New York: Plenum Press, 1987, p. 157–172.
 196. Willmott, N., J. K. Sethi, T. F. Walseth, H. C. Lee, A. M. White, and A. Galione. Nitric oxide‐induced mobilization of intracellular calcium via the cyclic ADP‐ribose signaling pathway. J. Biol. Chem. 271: 3699–3705, 1996.
 197. Wilt, F. H. Polyadenylation of maternal RNA of sea urchin eggs after fertilization. Proc. Natl. Acad. Sci. U.S.A. 70: 2345–2349, 1973.
 198. Winkler, M. M., and R. A. Steinhardt. Activation of protein synthesis in a sea urchin cell free system. Dev. Biol. 84: 432–439, 1981.
 199. Winkler, M. M., R. A. Steinhardt, J. L. Grainger, and L. Minning. Dual ionic controls for the activation of protein synthesis at fertilization. Nature 287: 558–560, 1980.
 200. Wistrom, C. A., and S. Meizel. Evidence suggesting involvement of a unique human sperm steroid receptor‐Cl‐ channel complex in the progesterone‐initiated acrosome reaction. Dev. Biol. 159: 679–690, 1993.
 201. Yamaguchi, M., M. Kurita, and N. Suzuki. Induction of the acrosome reaction of Hemicentrotus pulcherrimus spermatozoa by the egg jelly molecules, fucose‐rich glycoconjugate and sperm‐activating peptide I. Dev. Growth Diff. 31: 233–240, 1989.
 202. Yanagimachi, R., Mammalian fertilization. In: The Physiology Of Reproduction, (2nd ed.), edited by E. Knobil, and J. D. Neil. 1994, New York: Raven, vols. 1 and 2, Xxv + 1878 p. (vol. 1); Xxv + 1372 p. (vol. 2).
 203. Yoshino, K‐I., and N. Suzuki. Two classes of receptor specific for sperm‐activating peptide III in sand‐dollar spermatozoa. Eur. J. Biochem. 206: 887–893, 1992.
 204. Zucker, R. S., and R. A. Steinhardt. Prevention of the cortical reaction in fertilized sea urchin eggs by injection of calcium‐chelating ligands. Biochim. Biophys. Acta 541: 459–466, 1978.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

David Epel. Activation of Sperm and Egg During Fertilization. Compr Physiol 2011, Supplement 31: Handbook of Physiology, Cell Physiology: 859-884. First published in print 1997. doi: 10.1002/cphy.cp140123