Semin Reprod Med 2000; 18(2): 195-204
DOI: 10.1055/s-2000-12558
Copyright © 2000 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Regulation of Ionic Homeostasis by Mammalian Embryos

Michelle Lane, David K. Gardner
  • Colorado Center for Reproductive Medicine, Englewood, Colorado
Further Information

Publication History

Publication Date:
31 December 2000 (online)

ABSTRACT

Control and regulation of cellular homeostasis are essential for normal embryo development and maintenance of viability. By understanding the role of ionic homeostasis in normal cell development and homeostatic control by the developing embryo, it is possible to develop culture systems that minimize cellular stress and therefore maintain embryo viability. This article discusses the regulation of intracellular levels of protons (pHi), calcium, magnesium, and phosphate in mammalian embryos.

REFERENCES

  • 1 Johnson J D, Epel D, Paul M. Intracellular pH and activation of sea urchin eggs after fertilization.  Nature . 1976;  262 661-664
  • 2 Turin L, Warner A E. Intracellular pH in early Xenopus embryos: its effect on current flow between blastomeres.  J Physiol (Lond) . 1980;  300 489-504
  • 3 Bolsover S R, Silver R A, Whitaker M. Ratio imaging measurement of intracellular calcium and pH. In: Shotton D, ed. Electronic Light Microscopy: the Principles and Practice of Video-Enhanced Contrast, Digital Intensified Fluorescence, and Confocal Scanning Light Microscopy New York: Wiley-Liss 1993: 181-210
  • 4 Bright G R, Fisher G W, Rogowska J, Taylor D L. Fluorescence ratio imaging microscopy: temporal and spatial measurements of cytoplasmic pH.  J Cell Biol . 1987;  104 1019-1033
  • 5 Leclerc C, Becker D, Buehr M, Warner A. Low intracellular pH is involved in the early embryonic death of DDK mouse eggs fertilized by alien sperm.  Dev Dyn . 1994;  200 257-267
  • 6 Zhao Y, Chauvet P J, Alper S L, Baltz J M. Expression and function of bicarbonate/chloride exchangers in the preimplantation mouse embryo.  J Biol Chem . 1995;  270 24428-24434
  • 7 Zhao Y, Baltz J M. Bicarbonate/chloride exchange and intracellular pH throughout preimplantation mouse embryo development.  Am J Physiol . 1996;  271 C1512-C1520
  • 8 Lane M, Baltz J M, Bavister B D. Regulation of intracellular pH in hamster preimplantation embryos by the Na+/H+ antiporter.  Biol Reprod . 1998;  59 1483-1490
  • 9 Lane M, Baltz J M, Bavister B D. Na+/H+ antiporter activity in hamster embryos is activated during fertilization.  Dev Biol . 1999;  208 244-252
  • 10 Lane M, Bavister B D. Regulation of intracellular pH in bovine oocytes and cleavage stage embryos.  Mol Reprod Dev . 1999;  54 396-401
  • 11 Lee S C, Steinhardt R A. pH changes associated with meiotic maturation in oocytes of Xenopus laevis Dev Biol .  1981;  85 358-369
  • 12 Lee S C, Steinhardt R A. Observations on intracellular pH during cleavage of eggs of Xenopus laevis J Cell Biol .  1981;  91 414-419
  • 13 Webb D J, Nuccitelli R. Direct measurements of intracellular pH changes in Xenopus eggs at fertilization and cleavage.  J Cell Biol . 1981;  91 562-567
  • 14 Grandin N, Charbonneau M. Cycling of intracellular free calcium and intracellular pH in Xenopus embryos: a possible role in the control of the cell cycle.  J Cell Sci . 1991;  99 5-11
  • 15 Edwards L J, Batt P B, Williams D A, Gardner D K. pHi oscillations during bovine oocyte maturation.  Theriogenology . 1999;  51 369
  • 16 Phillips K P, Baltz J M. Intracellular pH regulation by HCO3-/Cl- exchange is activated during early mouse zygote development.  Dev Biol . 1999;  208 392-405
  • 17 Phillips K P, Leveille M C, Claman P, Baltz J M. Intracellular pH regulation in human preimplantation embryos.  Hum Reprod . 2000;  15 896-904
  • 18 Dale B, Menezo Y, Cohen J, DiMatteo L, Wilding M. Intracellular pH regulation in the human oocyte.  Hum Reprod . 1998;  13 964-970
  • 19 Boron W F, Roos A. Comparison of microelectrode, DMO, and methylamine methods for measuring intracellular pH.  Am J Physiol . 1976;  231 799-809
  • 20 Roos A, Boron W F. Intracellular pH.  Physiol Rev . 1981;  61 296-434
  • 21 Edwards L J, Williams D A, Gardner D K. Intracellular pH of the preimplantation mouse embryo: effects of extracellular pH and weak acids.  Mol Reprod Dev . 1998;  50 434-442
  • 22 Gibb C A, Poronnik P, Day M L, Cook D I. Control of cytosolic pH in two-cell mouse embryos: roles of H+-lactate cotransport and Na+/H+ exchange.  Am J Physiol . 1997;  273 C404-C419
  • 23 Miller J GO, Schultz G A. Amino acid content of preimplantation rabbit embryos and fluids of the reproductive tract.  Biol Reprod . 1987;  36 125
  • 24 Edwards L J, Williams D A, Gardner D K. Intracellular pH of the mouse preimplantation embryo: amino acids act as buffers of intracellular pH.  Hum Reprod . 1998;  13 3441-3448
  • 25 Kolajora M, Baltz J M. Volume-regulated anion and organic osmolyte channels in mouse zygotes.  Biol Reprod . 1999;  60 964-972
  • 26 Baltz J M, Biggers J D, Lechene C. Apparent absence of the Na+/H+ antiport activity in the two-cell mouse embryo.  Dev Biol . 1990;  138 421-429
  • 27 Baltz J M, Biggers J D, Lechene C. Two-cell stage mouse embryos appear to lack mechanisms for alleviating intracellular acid loads.  J Biol Chem . 1991;  266 6052-6057
  • 28 Barr K J, Garrill A, Jones D H, Orlowski J, Kidder G M. Contributions of Na+/H+ exchanger isoforms to preimplantation development of the mouse.  Mol Reprod Dev . 1998;  50 146-153
  • 29 Olsnes S, Tonnessen T I, Sandvig K. pH regulated anion antiport in nucleated mammalian cells.  J Cell Biol . 1986;  102 967-971
  • 30 Lane M, Baltz J M, Bavister B D. Bicarbonate/chloride exchange regulates intracellular pH of embryos but not oocytes of the hamster.  Biol Reprod . 1999;  61 452-457
  • 31 Miyazaki S, Igusa Y. Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations.  Nature . 1981;  290 706-707
  • 32 Jones K T, Carroll J, Merriman J A, Whittingham D G, Kono T. Repetitive sperm-induced Ca2+ transients in mouse oocytes are cell cycle dependent.  Development . 1995;  121 3259-3266
  • 33 Bos-Mikich A, Whittingham D G, Jones K T. Meiotic and mitotic Ca2+ oscillations affect cell composition in resulting blastocysts.  Dev Biol . 1997;  182 172-179
  • 34 Kline D, Zagray J A. Absence of an intracellular pH change following fertilization of the mouse egg.  Zygote . 1995;  3 305-311
  • 35 Salustri A, Yanagishita M, Underhill C B, Laurent T C, Hascall V C. Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle.  Dev Biol . 1992;  151 541-551
  • 36 Laurent C, Hellstrom S, Engstrom-Laurent A, Wells A F, Bergh A. Localization and quantity of hyaluronan in urogenital organs of male and female rats.  Cell Tissue Res . 1995;  279 241-248
  • 37 Begg D A, Rebhun L I. pH regulates the polymerization of actin in the sea urchin egg cortex.  J Cell Biol . 1979;  83 241-248
  • 38 Schatten G, Bestor T, Balczon R, Henson J, Schatten H. 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 . 1985;  36 116-127
  • 39 Begg D A, Wong G K, Hoyle D H, Baltz J M. Stimulation of cortical actin polymerization in the sea urchin egg cortex by NH4Cl, procaine and urethane: elevation of cytoplasmic pH is not the common mechanism of action.Cell Motil Cytoskeleton .  1996;  35 210-224
  • 40 Charbonneau M. The organization of the cortical endoplasmic reticulum in Xenopus eggs depends on intracellular pH: artefact of fixation or not?.  Cell Differ Dev . 1990;  30 171-179
  • 41 Squirrell J M, Lane M, Bavister B D. Development and cellular organization in preimplantation hamster embryos are disrupted by altering intracellular pH.  Dev Dyn. 2001;  In press
  • 42 Barnett D K, Bavister B D. Inhibitory effect of glucose and phosphate on the second cleavage division of hamster embryos: is it linked to metabolism?.  Hum Reprod . 1996;  11 177-183
  • 43 Biggers J D, Gardner D K, Leese H J. Control of carbohydrate metabolism on preimplantation embryos. In: Rosenblum IY, Heyner S, eds. Growth Factors in Mammalian Development Boca Raton, FL: CRC Press 1989: 19-36
  • 44 Leese H J. Metabolism of the preimplantation mammalian embryo. In: Milligan SR, ed. Oxford Reviews of Reproductive Biology Oxford: Oxford University Press 1992: 35
  • 45 Brinster R L, Thomson J L. Development of eight-cell mouse embryos in vitro.  Exp Cell Res . 1966;  42 308-315
  • 46 Seshagiri P B, Bavister B D. Glucose and phosphate inhibit respiration and oxidative metabolism in cultured hamster eight-cell embryos: evidence for the ``Crabtree effect''.  Mol Reprod Devel . 1991;  30 105-111
  • 47 Gardner D K, Lane M. The 2-cell block in CF1 mouse embryos is associated with an increase in glycolysis and a decrease in tricarboxylic acid (TCA) cycle activity: alleviation of the 2-cell block is associated with the restoration of in vivo metabolic pathway activities.  Biol Reprod . 1993;  48(suppl 1) 152
  • 48 Busa W B, Nuccitelli R. Metabolic regulation via intracellular pH.  Am J Physiol . 1984;  246 R409-R438
  • 49 McKhann G M, Tower D B. Ammonia toxicity and cerebral oxidative metabolism.  Am J Physiol . 1960;  200 420-424
  • 50 Paetkau V, Lardy H A. Phosphofructokinase: correlation of physical and enzymatic properties.  J Biol Chem . 1967;  242 2035-2042
  • 51 Danforth W H. Activation of glycolytic pathway in muscle. In: Chance B, Estabrook, RW, Williamson JB, eds. Control of Energy Metabolism New York: Academic Press 1965: 287-298
  • 52 Trivedi B, Danforth W H. Effect of pH on the kinetics of frog muscle phosphofructokinase.  J Biol Chem . 1966;  241 4110-4112
  • 53 Lane M, Lyons E A, Bavister B D. Cryopreservation reduces the ability of hamster 2-cell embryos to regulate intracellular pH.  Hum Reprod . 2000;  15 389-394
  • 54 Maunder C A, Yarom R, Dubowitz V. Electron-microscopic X-ray microanalysis of normal and diseased human muscle.  J Neurol Sci . 1977;  33 323-334
  • 55 Carafoli E, Crompton M. Calcium ion and mitochondria.  Sym Soc Exp Biol . 1976;  30 89-115
  • 56 Hales C N, Luzio J P, Chandler J A, Herman L. Localization of calcium in the smooth endoplasmic reticulum of rat isolated fat cells.  J Cell Sci . 1974;  15 1-15
  • 57 Campbell A K. Intracellular Calcium: Its Universal Role as a Regulator.  Chichester: John Wiley & Sons; 1983
  • 58 Parratt J R. Control and Manipulation of Calcium Movements.  New York: Raven Press; 1985
  • 59 Borland R M, Hazra S, Biggers J D, Lechene C P. The elemental composition of the environments of the gametes and preimplantation embryo during the initiation of pregnancy.  Biol Reprod . 1977;  16 147-157
  • 60 Borland R M, Biggers J D, Lechene C P, Taymour M L. Elemental composition of fluid in the human fallopian tube.  J Reprod Fertil . 1980;  58 479-482
  • 61 Casslen B, Nilsson B. Human uterine fluid, examined in undiluted samples for osmolarity and the concentrations of inorganic ions, albumin, glucose and urea.  Am J Obstet Gynecol . 1984;  150 877-881
  • 62 Rout U K, Krawetz S A, Armant D R. Ethanol-induced intracellular calcium mobilization rapidly alters gene expression in the mouse blastocyst.  Cell Calcium . 1997;  22 463-474
  • 63 Lane M, Bavister B D. Calcium homeostasis in early hamster preimplantation embryos.  Biol Reprod . 1998;  59 1000-1007
  • 64 Eisner D A, Lederer W J. Na-Ca exchange: stoichiometry and electrogenicity.  Am J Physiol . 1985;  248 C189-C202
  • 65 Borle A B. Na+-Ca2+ and Na+/H+ antiporter interactions. Relations between cytosolic free Ca2+, Na+ and intracellular pH. In: Pansu D, Bronner F, eds. Calcium Transport and Intracellular Calcium Homeostasis Berlin: Springer-Verlag 1990: 149-159
  • 66 Altura B M, Altura B T, Carella A, Turlapaty P D. Ca2+ coupling in vascular smooth muscle: Mg2+ and buffer effects on contractility and membrane Ca2+ movements.  Can J Physiol Pharmacol . 1982;  60 459-482
  • 67 Altura B M, Zhang A, Altura B T. Exposure of piglet coronary arterial muscle cells to low concentrations of Mg2+ found in blood of ischemic heart disease patients result in rapid elevation of cytosolic Ca2+: relevance to sudden infant death syndrome.  Eur J Pharmacol . 1997;  338 R7-R9
  • 68 Miyazaki S, Igusa Y. Ca-mediated activation of a K current at fertilization of golden hamster eggs.  Proc Natl Acad Sci U S A . 1982;  79 931-935
  • 69 Kaibara M, Mitarai S, Yano K A, Kameyama M. Involvement of Na+-H+ antiporter in regulation of L-type Ca2+ channel current by angiotensin II in rabbit ventricular myocytes.  Circ Res . 1977;  75 1121-1125
  • 70 Denton R M, McCormack J G, Edgell N J. Role of calcium ions in the regulation of intramitochondrial metabolism.  Effects of Na+, Mg2+, and ruthenium red on the Ca2+-stimulated oxidation of oxoglutarate and on pyruvate dehydrogenase activity in intact rat heart mitochondria. Biochem J . 1985;  190 107-117
  • 71 McCormack J G, Halestrap A P, Denton R M. Role of calcium ions in regulation of mammalian intramitochondrial metabolism.  Physiol Rev . 1990;  70 391-425
  • 72 Arnoult C, Kazam I G, Visconti P E, Kopf G S, Villaz M, Florman H M. Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation.  Proc Natl Acad Sci U S A . 1999;  96 6757-6762
  • 73 Abramczuk J, Solter D, Koprowski H. The beneficial effect EDTA on development of mouse one-cell embryos in chemically defined medium.  Dev Biol . 1977;  61 378-383
  • 74 Chatot C L, Ziomek C A, Bavister B D, Lewis J L, Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro.  J Reprod Fertil . 1989;  86 679-688
  • 75 Quinn P. Enhanced results in mouse and human embryo culture using a modified human tubal fluid medium lacking glucose and phosphate.  J Assist Reprod Genet . 1995;  12 97-105
  • 76 Gardner D K, Lane M. Alleviation of the ``2-cell block'' and development to the blastocyst of CF1 mouse embryos: role of amino acids, EDTA and physical parameters.  Hum Reprod . 1996;  11 2703-2712
  • 77 Lane M, Gardner D K. EDTA stimulates development of cleavage stage mouse embryos by inhibiting the glycolytic enzyme 3-phosphoglycerate kinase.  Biol Reprod . 1997;  56(suppl) 26(abstract)
  • 78 Cunningham D D, Pardee A B. Transport changes rapidly initiated by serum addition to ``contact inhibited'' 3T3 cells.  Proc Natl Acad Sci U S A . 1969;  64 1049-1056
  • 79 Crabtree H G. Observations on the carbohydrate metabolism of tumours.  Biochem J . 1929;  23 536-545
  • 80 Schini S A, Bavister B D. Two-cell block to development of cultured hamster embryos is caused by phosphate and glucose.  Biol Reprod . 1998;  39 1183-1192
  • 81 Seshagiri P B, Bavister B D. Phosphate is required for inhibition by glucose of development of hamster 8-cell embryos in vitro.  Biol Reprod . 1989;  40 607-614
  • 82 Gardner D K, Lane M, Spitzer A, Batt P A. Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins and culturing embryos in groups stimulate development.  Biol Reprod . 1994;  50 390-400
  • 83 Meyer M, Seshagiri P B. Analysis of phosphate-inhibition of development of hamster 2-cell embryos in vitro.  Biol Reprod . 1990;  42(suppl 1) 48
    >