Cell volume regulation in mammalian oocytes and preimplantation embryos

Molecular Reproduction and Development

Volumn 79, Issue 12, 2012, Pages 821-831

  Baltz, Jay M ^a,b,c   Zhou, Chenxi ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ALANINE; BETAINE; BICARBONATE SODIUM COTRANSPORTER; CHLORIDE CHANNEL; GLYCINE; GLYCINE TRANSPORTER 1; JANUS KINASE 2; POTASSIUM CHANNEL; SODIUM PROTON EXCHANGE PROTEIN;

CELL ADHESION; CELL VOLUME; EMBRYO DEVELOPMENT; FERTILIZATION; GERMINAL VESICLE; HUMAN; NIDATION; NONHUMAN; OOCYTE; OSMOLALITY; PRIORITY JOURNAL; REVIEW; ZONA PELLUCIDA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLASTOCYST; CELL SIZE; FEMALE; GLYCINE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; MEMBRANE PROTEINS; OOCYTES; OSMOLAR CONCENTRATION; OVARIAN FOLLICLE; WATER-ELECTROLYTE BALANCE; ZONA PELLUCIDA;

MAMMALIA;

EID: 84870879207     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22117     Document Type: Review

References (99)

1. Alexander RT, Grinstein S. 2006. Na+/H+ exchangers and the regulation of volume. Acta Physiol (Oxf) 187: 159- 167.
2. Alper SL. 2006. Molecular physiology of SLC4 anion exchangers. Exp Physiol 91: 153- 161.
3. Anas MKI, Hammer MA, Lever M, Stanton JA, Baltz JM. 2007. The organic osmolytes betaine and proline are transported by a shared system in early preimplantation mouse embryos. J Cell Physiol 210: 266- 277.
4. Anas MK, Lee MB, Zhou C, Hammer MA, Slow S, Karmouch J, Liu XJ, Broer S, Lever M, Baltz JM. 2008. SIT1 is a betaine/proline transporter that is activated in mouse eggs after fertilization and functions until the 2-cell stage. Development 135: 4123- 4130.
5. Baltz JM. 2001. Osmoregulation and cell volume regulation in the preimplantation embryo. Schatten GP, editor. Current topics in developmental biology. San Diego: Academic Press. pp 55- 106.
6. Baltz JM, Tartia AP. 2010. Cell volume regulation in oocytes and early embryos: Connecting physiology to successful culture media. Hum Reprod Update 16: 166- 176.
7. Baltz JM, Biggers JD, Lechene C. 1991. Relief from alkaline load in two-cell stage mouse embryos by bicarbonate/chloride exchange. J Biol Chem 266: 17212- 17217.
8. Bell CE, Lariviere NM, Watson PH, Watson AJ. 2009. Mitogen-activated protein kinase (MAPK) pathways mediate embryonic responses to culture medium osmolarity by regulating Aquaporin 3 and 9 expression and localization, as well as embryonic apoptosis. Hum Reprod 24: 1373- 1386.
9. Biggers JD. 1998. Reflections on the culture of the preimplantation embryo. Int J Dev Biol 42: 879- 884.
10. Biggers JD, Lawitts JA, Lechene CP. 1993. The protective action of betaine on the deleterious effects of NaCl on preimplantation mouse embryos in vitro. Mol Reprod Dev 34: 380- 390.
11. Bolton VN, Hawes SM, Taylor CT, Parsons JH. 1989. Development of spare human preimplantation embryos in vitro: An analysis of the correlations among gross morphology, cleavage rates, and development to the blastocyst. J In Vitro Fert Embryo Transf 6: 30- 35.
12. Borowsky B, Hoffman BJ. 1998. Analysis of a gene encoding two glycine transporter variants reveals alternative promoter usage and a novel gene structure. J Biol Chem 273: 29077- 29085.
13. Camous S, Heyman Y, Meziou W, Menezo Y. 1984. Cleavage beyond the block stage and survival after transfer of early bovine embryos cultured with trophoblastic vesicles. J Reprod Fertil 72: 479- 485.
14. Cetinkaya A, Erdogan S. 2008. Changes of HCO3-/Cl- exchanger activity during meiotic maturation in Balb/c strain mouse oocytes and zygotes. J Reprod Dev 54: 492- 495.
15. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I. 1989. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 86: 679- 688.
16. Chen NH, Reith ME, Quick MW. 2004. Synaptic uptake and beyond: The sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflugers Arch 447: 519- 531.
17. Collins JL, Baltz JM. 1999. Estimates of mouse oviductal fluid tonicity based on osmotic responses of embryos. Biol Reprod 60: 1188- 1193.
18. Dandekar P, Talbot P. 1992. Perivitelline space of mammalian oocytes: Extracellular matrix of unfertilized oocytes and formation of a cortical granule envelope following fertilization. Mol Reprod Dev 31: 135- 143.
19. Dawson KM, Baltz JM. 1997. Organic osmolytes and embryos: Substrates of the Gly and beta transport systems protect mouse zygotes against the effects of raised osmolarity. Biol Reprod 56: 1550- 1558.
20. Dawson KM, Collins JL, Baltz JM. 1998. Osmolarity-dependent glycine accumulation indicates a role for glycine as an organic osmolyte in early preimplantation mouse embryos. Biol Reprod 59: 225- 232.
21. Erdogan S, Cetinkaya A, Tuli A, Yilmaz ED, Dogan A. 2011. Changes in the activity of defense mechanisms against induced acidosis during meiotic maturation in mouse oocytes. Theriogenology 75: 1057- 1066.
22. Fiorenza MT, Bevilacqua A, Canterini S, Torcia S, Pontecorvi M, Mangia F. 2004. Early transcriptional activation of the hsp70.1 gene by osmotic stress in one-cell embryos of the mouse. Biol Reprod 70: 1606- 1613.
23. Garcia-Perez A, Burg MB. 1991. Role of organic osmolytes in adaptation of renal cells to high osmolality. J Membr Biol 119: 1- 13.
24. Garnovskaya MN, Mukhin YV, Vlasova TM, Raymond JR. 2003. Hypertonicity activates Na+/H+ exchange through Janus kinase 2 and calmodulin. J Biol Chem 278: 16908- 16915.
25. Gatsios P, Terstegen L, Schliess F, H+ñussinger D, Kerr IM, Heinrich PC, Graeve L. 1998. Activation of the janus kinase/signal transducer and activator of transcription pathway by osmotic shock. J Biol Chem 273: 22962- 22968.
26. Gibb CA, Poronnik P, Day ML, Cook DI. 1997. Control of cytosolic pH in two-cell mouse embryos: Roles of H(+)-lactate cotransport and Na+/H+ exchange. Am J Physiol 273: C404- C419.
27. Goddard MJ, Pratt HPM. 1983. Control of events during early cleavage of the mouse embryo: An analysis of the "2-cell block". Development 73: 111- 133.
28. Grinstein S, Woodside M, Sardet C, Pouyssegur J, Rotin D. 1992. Activation of the Na+/H+ antiporter during cell volume regulation. Evidence for a phosphorylation-independent mechanism. J Biol Chem 267: 23823- 23828.
29. Guastella J, Brecha N, Weigmann C, Lester HA, Davidson N. 1992. Cloning, expression, and localization of a rat brain high-affinity glycine transporter. Proc Natl Acad Sci USA 89: 7189- 7193.
30. Guerin JF, Gallois E, Croteau S, Revol N, Maurin F, Guillaud J, Menezo Y. 1995. Techniques de récolte et aminogrammes des liquides tubaire et folliculaire chez les femelles domestiques. Revue Med Vet 146: 805- 814.
31. Hadi T, Hammer MA, Algire C, Richards T, Baltz JM. 2005. Similar effects of osmolarity, glucose, and phosphate on cleavage past the 2-cell stage in mouse embryos from outbred and F1 hybrid females. Biol Reprod 72: 179- 187.
32. Hallows KR, Knauf PA. 1994. Principles of cell volume regulation. Strange K, editor. Cellular and molecular physiology of cell volume regulation. Boca Raton: CRC Press. pp 3- 29.
33. Hammer MA, Baltz JM. 2002. Betaine is a highly effective organic osmolyte but does not appear to be transported by established organic osmolyte transporters in mouse embryos. Mol Reprod Dev 62: 195- 202.
34. Hammer MA, Baltz JM. 2003. Beta-alanine but not taurine can function as an organic osmolyte in preimplantation mouse embryos cultured from fertilized eggs. Mol Reprod Dev 66: 153- 161.
35. Hammer MA, Kolajova M, Leveille M, Claman P, Baltz JM. 2000. Glycine transport by single human and mouse embryos. Hum Reprod 15: 419- 426.
36. Harding EA, Gibb CA, Johnson MH, Cook DI, Day ML. 2002. Developmental changes in the management of acid loads during preimplantation mouse development. Biol Reprod 67: 1419- 1429.
37. Harris SE, Gopichandran N, Picton HM, Leese HJ, Orsi NM. 2005. Nutrient concentrations in murine follicular fluid and the female reproductive tract. Theriogenology 64: 992- 1006.
38. Hoffmann EK, Lambert IH, Pedersen SF. 2009. Physiology of cell volume regulation in vertebrates. Physiol Rev 89: 193- 277.
39. Humphreys BD, Jiang L, Chernova MN, Alper SL. 1995. Hypertonic activation of AE2 anion exchanger in Xenopus oocytes via NHE-mediated intracellular alkalinization. Am J Physiol 268: C201- C209.
40. Inoue A, Akiyama T, Nagata M, Aoki F. 2007. The perivitelline space-forming capacity of mouse oocytes is associated with meiotic competence. J Reprod Dev 53: 1043- 1052.
41. Jamshidi MB, Kaye PL. 1995. Glutamine transport by mouse inner cell masses. J Reprod Fertil 104: 91- 97.
42. Jiang L, Chernova MN, Alper SL. 1997. Secondary regulatory volume increase conferred on Xenopus oocytes by expression of AE2 anion exchanger. Am J Physiol 272: C191- C202.
43. Kempf B, Bremer E. 1998. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170: 319- 330.
44. Kishi J, Noda Y, Narimoto K, Umaoka Y, Mori T. 1991. Block to development in cultured rat 1-cell embryos is overcome using medium HECM-1. Hum Reprod 6: 1445- 1448.
45. Knudsen JF, Litkowski LJ, Wilson TL, Guthrie HD, Batta SK. 1979. Follicular fluid electrolytes and osmolality in cyclic pigs. J Reprod Fertil 57: 419- 422.
46. Kolajova M, Baltz JM. 1999. Volume-regulated anion and organic osmolyte channels in mouse zygotes. Biol Reprod 60: 964- 972.
47. Kolajova M, Hammer MA, Collins JL, Baltz JM. 2001. Developmentally regulated cell cycle dependence of swelling-activated anion channel activity in the mouse embryo. Development 128: 3427- 3434.
48. Krump E, Nikitas K, Grinstein S. 1997. Induction of tyrosine phosphorylation and Na+/H+ exchanger activation during shrinkage of human neutrophils. J Biol Chem 272: 17303- 17311.
49. Kwon HM, Handler JS. 1995. Cell volume regulated transporters of compatible osmolytes. Curr Opin Cell Biol 7: 465- 471.
50. Lane M, Bavister BD. 1999. Regulation of intracellular pH in bovine oocytes and cleavage stage embryos. Mol Reprod Dev 54: 396- 401.
51. Lane M, Baltz JM, Bavister BD. 1998. Regulation of intracellular pH in hamster preimplantation embryos by the sodium hydrogen (Na+/H+) antiporter. Biol Reprod 59: 1483- 1490.
52. Lane M, Baltz JM, Bavister BD. 1999a. Bicarbonate/chloride exchange regulates intracellular pH of embryos but not oocytes of the hamster. Biol Reprod 61: 452- 457.
53. Lane M, Baltz JM, Bavister BD. 1999b. Na+/H+ antiporter activity in hamster embryos is activated during fertilization. Dev Biol 208: 244- 252.
54. Lang F, Busch GL, Volkl H. 1998. The diversity of volume regulatory mechanisms. Cell Physiol Biochem 8: 1- 45.
55. Lawitts JA, Biggers JD. 1991a. Optimization of mouse embryo culture media using simplex methods. J Reprod Fertil 91: 543- 556.
56. Lawitts JA, Biggers JD. 1991b. Overcoming the 2-cell block by modifying standard components in a mouse embryo culture medium. Biol Reprod 45: 245- 251.
57. Lawitts JA, Biggers JD. 1992. Joint effects of sodium chloride, glutamine, and glucose in mouse preimplantation embryo culture media. Mol Reprod Dev 31: 189- 194.
58. Lawitts JA, Biggers JD. 1993. Culture of preimplantation embryos. Methods Enzymol 225: 153- 164.
59. Lewis AM, Kaye PL. 1992. Characterization of glutamine uptake in mouse two-cell embryos and blastocysts. J Reprod Fertil 95: 221- 229.
60. Li R, Whitworth K, Lai L, Wax D, Spate L, Murphy CN, Rieke A, Isom C, Hao Y, Zhong Z, Katayama M, Schatten H, Prather RS. 2007. Concentration and composition of free amino acids and osmolalities of porcine oviductal and uterine fluid and their effects on development of porcine IVF embryos. Mol Reprod Dev 74: 1228- 1235.
61. Okada Y. 1997. Volume expansion-sensing outward-rectifier Cl- channel: Fresh start to the molecular identity and volume sensor. Am J Physiol 273: C755- C789.
62. Orlowski J, Grinstein S. 2004. Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch 447: 549- 565.
63. Pastor-Anglada M, Felipe A, Casado FJ, Ferrer-Martinez A, Gomez-Angelats M. 1996. Long-term osmotic regulation of amino acid transport systems in mammalian cells. Amino Acids 11: 135- 151.
64. - exchange is activated during early mouse zygote development. Dev Biol 208: 392- 405.
65. Phillips KP, Leveille MC, Claman P, Baltz JM. 2000. Intracellular pH regulation in human preimplantation embryos. Hum Reprod 15: 896- 904.
66. - exchanger in the mouse oocyte is inactivated during first meiotic metaphase and reactivated after egg activation via the MAP kinase pathway. Mol Biol Cell 13: 3800- 3810.
67. Prather RS. 2010. Whatever happened to the "cell-block" during mammalian embryogenesis? Mol Reprod Dev 77(5): DOI: 10.1002/mrd.21182.
68. Richards T, Wang F, Liu L, Baltz JM. 2010. Rescue of postcompaction-stage mouse embryo development from hypertonicity by amino acid transporter substrates that may function as organic osmolytes. Biol Reprod 82: 769- 777.
69. Romero MF, Fulton CM, Boron WF. 2004. The SLC4 family of HCO(3)(-) transporters. Pflugers Arch 447: 495- 509.
70. Schini SA, Bavister BD. 1988. Two-cell block to development of cultured hamster embryos is caused by phosphate and glucose. Biol Reprod 39: 1183- 1192.
71. Schultz GA, Kaye PL, McKay DJ, Johnson MH. 1981. Endogenous amino acid pool sizes in mouse eggs and preimplantation embryos. J Reprod Fertil 61: 387- 393.
72. Seguin DG, Baltz JM. 1997. Cell volume regulation by the mouse zygote: Mechanism of recovery from a volume increase. Am J Physiol 272: C1854- C1861.
73. Sloan JL, Mager S. 1999. Cloning and functional expression of a human Na(+) and Cl(-)-dependent neutral and cationic amino acid transporter B(0+). J Biol Chem 274: 23740- 23745.
74. Sonoda M, Okamoto F, Kajiya H, Inoue Y, Honjo K, Sumii Y, Kawarabayashi T, Okabe K. 2003. Amino acid-permeable anion channels in early mouse embryos and their possible effects on cleavage. Biol Reprod 68: 947- 953.
75. Steeves CL, Baltz JM. 2005. Regulation of intracellular glycine as an organic osmolyte in early preimplantation mouse embryos. J Cell Physiol 204: 273- 279.
76. + antiporter among 2-cell mouse embryos derived from females of different strains. Biol Reprod 65: 14- 22.
77. Steeves CL, Hammer MA, Walker GB, Rae D, Stewart NA, Baltz JM. 2003. The glycine neurotransmitter transporter GLYT1 is an organic osmolyte transporter regulating cell volume in cleavage-stage embryos. Proc Natl Acad Sci USA 100: 13982- 13987.
78. Strange K, Emma F, Jackson PS. 1996. Cellular and molecular physiology of volume-sensitive anion channels. Am J Physiol 270: C711- C730.
79. Talbot P, Dandekar P. 2003. Perivitelline space: Does it play a role in blocking polyspermy in mammals? Microsc Res Tech 61: 349- 357.
80. Tartia AP, Rudraraju N, Richards T, Hammer MA, Talbot P, Baltz JM. 2009. Cell volume regulation is initiated in mouse oocytes after ovulation. Development 136: 2247- 2254.
81. Van Winkle LJ, Campione AL. 1996. Amino acid transport regulation in preimplantation mouse embryos: Effects on amino acid content and pre- and peri-implantation development. Theriogenology 45: 69- 80.
82. Van Winkle LJ, Dickinson HR. 1995. Differences in amino acid content of preimplantation mouse embryos that develop in vitro versus in vivo: In vitro effects of five amino acids that are abundant in oviductal secretions. Biol Reprod 52: 96- 104.
83. Van Winkle LJ, Haghighat N, Campione AL, Gorman JM. 1988. Glycine transport in mouse eggs and preimplantation conceptuses. Biochim Biophys Acta 941: 241- 256.
84. Van Winkle LJ, Campione AL, Farrington BH. 1990a. Development of system B0, + and a broad-scope Na(+)-dependent transporter of zwitterionic amino acids in preimplantation mouse conceptuses. Biochim Biophys Acta 1025: 225- 233.
85. Van Winkle LJ, Haghighat N, Campione AL. 1990b. Glycine protects preimplantation mouse conceptuses from a detrimental effect on development of the inorganic ions in oviductal fluid. J Exp Zool 253: 215- 219.
86. Van Winkle LJ, Patel M, Wasserlauf HG, Dickinson HR, Campione AL. 1994. Osmotic regulation of taurine transport via system beta and novel processes in mouse preimplantation conceptuses. Biochim Biophys Acta 1191: 244- 255.
87. Wang F, Kooistra M, Lee M, Liu L, Baltz JM. 2011. Mouse embryos stressed by physiological levels of osmolarity become arrested in the late 2-cell stage before entry into M phase. Biol Reprod 85: 702- 713.
88. Waring DW. 1976. Rate of formation and osmolality of oviductal fluid in the cycling rat. Biol Reprod 15: 297- 302.
89. Waymouth C. 1970. Osmolality of mammalian blood and of media for culture of mammalian cells. In Vitro 6: 109- 127.
90. Wehner F, Olsen H, Tinel H, Kinne-Saffran E, Kinne RK. 2003. Cell volume regulation: Osmolytes, osmolyte transport, and signal transduction. Rev Physiol Biochem Pharmacol 148: 1- 80.
91. Whittingham DG. 1971. Culture of mouse ova. J Reprod Fertil Suppl 14: 7- 21.
92. Williams N, Kraft N, Shortman K. 1972. The separation of different cell classes from lymphoid organs. VI. The effect of osmolarity of gradient media on the density distribution of cells. Immunology 22: 885- 899.
93. Xie Y, Zhong W, Wang Y, Trostinskaia A, Wang F, Puscheck EE, Rappolee DA. 2007. Using hyperosmolar stress to measure biologic and stress-activated protein kinase responses in preimplantation embryos. Mol Hum Reprod 13: 473- 481.
94. Yancey PH. 1994. Compatible and counteracting solutes. Strange K, editor. Cellular and molecular physiology of cell volume regulation. Boca Raton, FL: CRC Press. pp 81- 109.
95. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN. 1982. Living with water stress: Evolution of osmolyte systems. Science 217: 1214- 1222.
96. Zhao Y, Baltz JM. 1996. Bicarbonate/chloride exchange and intracellular pH throughout preimplantation mouse embryo development. Am J Physiol 271: C1512- C1520.
97. Zhao Y, Chauvet PJ, Alper SL, Baltz JM. 1995. Expression and function of bicarbonate/chloride exchangers in the preimplantation mouse embryo. J Biol Chem 270: 24428- 24434.
98. Zhou C, Baltz JM. 2012. Janus kinase 2 mediates the acute response to a cell volume decrease in mouse preimplantation embryos by activating Na(+)/H(+) exchanger isoform 1. J Cell Physiol.
99. Zhou C, Tiberi M, Liang B, Alper SL, Baltz JM. 2009. HCO3(-)/Cl(-) exchange inactivation and reactivation during mouse oocyte meiosis correlates with MEK/MAPK-regulated Ae2 plasma membrane localization. PLoS ONE 4: e7417.