JAK2 mediates the acute response to decreased cell volume in mouse preimplantation embryos by activating NHE1

Journal of Cellular Physiology

Volumn 228, Issue 2, 2013, Pages 428-438

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

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARIPORIDE; GENISTEIN; JANUS KINASE 2; SODIUM PROTON EXCHANGE PROTEIN 1;

ACUTE STRESS; ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL VOLUME; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; IONIC STRENGTH; MOUSE; NONHUMAN; OSMOLARITY; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; BLASTOCYST; CALMODULIN; CATION TRANSPORT PROTEINS; CELL SIZE; FEMALE; GENISTEIN; GUANIDINES; JANUS KINASE 2; MALE; MICE; PHOSPHORYLATION; PREGNANCY; PROTEIN KINASE INHIBITORS; SODIUM-HYDROGEN ANTIPORTER; SULFONES; SUPEROVULATION; TYPE C PHOSPHOLIPASES; TYROSINE;

EID: 84868019287     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24147     Document Type: Article

References (57)

1. + 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. 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.
4. 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.
5. + exchanger isoforms to preimplantation development of the mouse. Mol Reprod Dev 50:146-153.
6. Behrmann I, Smyczek T, Heinrich PC, Schmitz-Van de Leur H, Komyod W, Giese B, Muller-Newen G, Haan S, Haan C. 2004. Janus kinase (Jak) subcellular localization revisited: The exclusive membrane localization of endogenous Janus kinase 1 by cytokine receptor interaction uncovers the Jak. receptor complex to be equivalent to a receptor tyrosine kinase. J Biol Chem 279:35486-35493.
7. + exchanger isoform 1 (NHE1) is a novel member of the calmodulin-binding proteins. Identification and characterization of calmodulin-binding sites. J Biol Chem 269:13703-13709.
8. + exchanger isoform NHE4 in rat thick ascending limbs. Am J Physiol Renal Physiol 281:F707-F717.
9. Coaxum SD, Garnovskaya MN, Gooz M, Baldys A, Raymond JR. 2009. Epidermal growth factor activates Na(+/)H(+) exchanger in podocytes through a mechanism that involves Janus kinase and calmodulin. Biochim Biophys Acta 1793:1174-1181.
10. Collins JL, Baltz JM. 1999. Estimates of mouse oviductal fluid tonicity based on osmotic responses of embryos. Biol Reprod 60:1188-1193.
11. 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.
12. 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.
13. Erdogan S, FitzHarris G, Tartia AP, Baltz JM. 2005. Mechanisms regulating intracellular pH are activated during growth of the mouse oocyte coincident with acquisition of meiotic competence. Dev Biol 286:352-360.
14. Feng J, Witthuhn BA, Matsuda T, Kohlhuber F, Kerr IM, Ihle JN. 1997. Activation of Jak2 catalytic activity requires phosphorylation of Y1007 in the kinase activation loop. Mol Cell Biol 17:2497-2501.
15. 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.
16. FitzHarris G, Baltz JM. 2006. Granulosa cells regulate intracellular pH of the murine growing oocyte via gap junctions: Development of independent homeostasis during oocyte growth. Development 133:591-599.
17. FitzHarris G, Siyanov V, Baltz JM. 2007. Granulosa cells regulate oocyte intracellular pH against acidosis in preantral follicles by multiple mechanisms. Development 134:4283-4295.
18. Fong B, Watson PH, Watson AJ. 2007. Mouse preimplantation embryo responses to culture medium osmolarity include increased expression of CCM2 and p38 MAPK activation. BMC Dev Biol 7:2.
19. 2+ and PKC{delta} for Janus Kinase 2 Activation by Angiotensin II: Involvement of PYK2. Mol Endocrinol 16:367-377.
20. Garcia-Perez A, Burg MB. 1991. Renal medullary organic osmolytes. Physiol Rev 71:1081-1115.
21. + exchange through Janus kinase 2 and calmodulin. J Biol Chem 278:16908-16915.
22. 2+/calmodulin. Biochemistry 42:7178-7187.
23. Gatsios P, Terstegen L, Schliess F, Häussinger 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.
24. + antiporter during cell volume regulation. Evidence for a phosphorylation-independent mechanism. J Biol Chem 267:23823-23828.
25. Haan C, Kroy DC, Wuller S, Sommer U, Nocker T, Rolvering C, Behrmann I, Heinrich PC, Haan S. 2009. An unusual insertion in Jak2 is crucial for kinase activity and differentially affects cytokine responses. J Immunol 182:2969-2977.
26. 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.
27. Hoffmann EK, Lambert IH, Pedersen SF. 2009. Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193-277.
28. 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.
29. Ito M, Nakasato M, Suzuki T, Sakai S, Nagata M, Aoki F. 2004. Localization of Janus kinase 2 to the nuclei of mature oocytes and early cleavage stage mouse embryos. Biol Reprod 71:89-96.
30. 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.
31. Junger WG, Hoyt DB, Davis RE, Herdon-Remelius C, Namiki S, Junger H, Loomis W, Altman A. 1998. Hypertonicity regulates the function of human neutrophils by modulating chemoattractant receptor signaling and activating mitogen-activated protein kinase p38. J Clin Invest 101:2768-2779.
32. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, Faraoni R, Floyd M, Hunt JP, Lockhart DJ, Milanov ZV, Morrison MJ, Pallares G, Patel HK, Pritchard S, Wodicka LM, Zarrinkar PP. 2008. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 26:127-132.
33. Kisseleva T, Bhattacharya S, Braunstein J, Schindler CW. 2002. Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene 285:1-24.
34. + exchanger activation during shrinkage of human neutrophils. J Biol Chem 272:17303-17311.
35. Lang F, Busch GL, Volkl H. 1998. The diversity of volume regulatory mechanisms. Cell Physiol Biochem 8:1-45.
36. 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.
37. Lawitts JA, Biggers JD. 1993. Culture of preimplantation embryos. Methods Enzymol 225:153-164.
38. + exchanger. Can J Physiol Pharmacol 84:1081-1095.
39. Masereel B, Pochet L, Laeckmann D. 2003. An overview of inhibitors of Na(+)/H(+) exchanger. Eur J Med Chem 38:547-554.
40. Matsuda T, Feng J, Witthuhn BA, Sekine Y, Ihle JN. 2004. Determination of the transphosphorylation sites of Jak2 kinase. Biochem Biophys Res Commun 325:586-594.
41. Nakasato M, Shirakura Y, Ooga M, Iwatsuki M, Ito M, Kageyama S, Sakai S, Nagata M, Aoki F. 2006. Involvement of the STAT5 signaling pathway in the regulation of mouse preimplantation development. Biol Reprod 75:508-517.
42. Orlowski J, Grinstein S. 2004. Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch 447:549-565.
43. Romero MF, Fulton CM, Boron WF. 2004. The SLC4 family of HCO(3)(-) transporters. Pflugers Arch 447:495-509.
44. + exchanger subtype 3 in various cell types. Pflugers Arch 436:797-800.
45. Steeves CL, Baltz JM. 2005. Regulation of intracellular glycine as an organic osmolyte in early preimplantation mouse embryos. J Cell Physiol 204:273-279.
46. 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.
47. Szaszi K, Buday L, Kapus A. 1997. Shrinkage-induced protein tyrosine phosphorylation in Chinese hamster ovary cells. J. Biol Chem 272:16670-16678.
48. 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.
49. Thomas JA, Buchsbaum RN, Zimniak A, Racker E. 1979. Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18:2210-2218.
50. 2+-calmodulin and Janus kinase 2 are required for activation of sodium-proton exchange by the Gi-coupled 5-hydroxytryptamine 1a receptor. J Pharmacol Exp Ther 320:314-322.
51. 2+ regulation-defective. J Biol Chem 269:13710-13715.
52. 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.
53. 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.
54. Wilks AF. 2008. The JAK kinases: Not just another kinase drug discovery target. Semin Cell Dev Biol 19:319-328.
55. 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.
56. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN. 1982. Living with water stress: Evolution of osmolyte systems. Science 217:1214-1222.
57. 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.