Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro

Duygu Mutluay; Hakan Öner

Research Article

Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro

Year 2019, Volume: 66 Issue: 1, 89 - 93, 31.12.2018

Duygu Mutluay , Hakan Öner

Abstract

The c-Abl gene is a nonreceptor tyrosine kinase that has roles in cell growth, control of the cell cycle, initiation of
pronuclear movement and actin cytoskeleton dynamics. The present study has examined the localization of c-Abl protein during oocyte
activation in mouse in vitro. Confocal immunofluorescence analysis showed that c-Abl originates at the cortex with a crescent shape
before the activation and continues up along both sides of the cortex after activation during meiotic division until pronuclear stage.
These results demonstrate that c-Abl may play role in asymmetric division of the egg to produce polar body, positioning of the spindle,
and may regulate the microtubule cytoskeleton or have some roles in this process.

Keywords

c-Abl, meiotic division, oocyte activation, spindle positioning

References

1. Abelson HT, Rabstein LS (1970): Lymphosarcoma: virusinduced thymic-independent disease in mice. Cancer Res, 30, 2213-2222.
2. Ahmad K, Naz RK (1994): Protein phosphorylation pattern and role of products of c-erbB-1 and c-abl protooncogenes in murine preimplantation embryonic development. Am J Reprod Immunol, 32, 226–237.
3. Ben-Neriah Y, Daley GQ, Mes-Masson AM, et al. (1986): The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science, 233, 212– 214.
4. Bradley WD, Koleske AJ (2009): Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts. J. Cell Sci, 122, 3441–3454.
5. Brunet S, Maro B (2005): Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction, 130, 801-811.
6. Colicelli J (2011): ABL tyrosine kinases: evolution of function, regulation, and specificity. Sci Signal, 4(188):er4.
7. Diaz H, Esponda P (2004): Ageing-induced changes in the cortical granules of mouse eggs. Zygote, 12, 95–103.
8. Goff SP, Gilboa E, Witte ON, et al. (1980): Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell, 22, 777–785.
9. Gonzalez C (2007): Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nature Rev Genet, 8, 462–472.
10. Greuber EK, Smith-Pearson P, Wang J, et al. (2013): Role of ABL family kinases in cancer: from leukaemia to solid tumours. Nat Rev Cancer, 13, 559-571.
11. Hantschel O, Superti-Furga G (2004): Regulation of the c Abl and Bcr-Abl tyrosine kinases. Nature Rev Mol Cell Biol, 5, 33–44.
12. Hernandez SE, Krishnaswami M, Miller AL, et al. (2004): How do Abl family kinases regulate cell shape and movement? Trends Cell Biol, 4, 36-44.
13. Iwaoki Y, Matsuda H, Mutter GL, et al. (1993): Differential expression of the proto-oncogenes c-abl and cmos in developing mouse germ cells. Exp Cell Res, 206, 212–219.
14. Li B, Boast S, de los Santos K, et al. (2000): Mice deficient in Abl are osteoporotic and have defects in osteoblast maturation. Nature Genet, 24, 304–308.
15. Ma SF, Liu XY, Miao DQ, et al. (2005): Parthenogenetic activation of mouse oocytes by strontium chloride: a search for the best conditions. Theriogenology, 64, 1142-1157.
16. Maro B, Verlhac MH (2002): Polar body formation: new rules for asymmetric divisions. Nat Cell Biol, 4, E281-3.
17. Matsumura S, Hamasaki M, Yamamoto T, et al. (2012): ABL1 regulates spindle orientation in adherent cells and mammalian skin. Nat Commun, 3, 626.
18. Moore KL, Kinsey WH (1994): Identification of an ablrelated protein tyrosine kinase in the cortex of the sea urchin egg: possible role at fertilization. Dev Biol, 164, 444–455.
19. Moore KL, Kinsey WH (1995): Effects of protein tyrosine kinase inhibitors on egg activation and fertilizationdependent protein tyrosine kinase activity. Dev Biol, 168, 1-10.
20. Mutluay D (2016): Distribution of primitive endoderm and epiblast lineage specific factors in late stage blastocysts. Slov Vet Res, 53, 211-217.
21. Mutluay D, Oner H (2017): The Abelson tyrosine kinase (c-Abl) Localization in Preimplantation Mouse Development. Rom J Morphol Embryol, 58, 1385-1391.
22. Nagy A, Gertsenstein M, Vintersten K, et al. (2003): Collection of zygotes and removal of cumulus cells with hyluronidase. 139-142. In: Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
23. Tybulewicz VL, Crawford CE, Jackson PK, et al. (1991): Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell, 65, 1153–1163.
24. Walker G, Burgess D, Kinsey WH (1996): Fertilization promotes selective association of the Abl [correction of AbI] kinase with the egg cytoskeleton. Eur J Cell Biol, 70, 165- 171.
25. Wang JY (2014): The capable ABL: what is its biological function? Mol Cell Biol, 34, 1188-1197.
26. Webb M, Howlett SK, Maro B (1986): Parthenogenesis and cytoskeletal organization in ageing mouse eggs. J Embryol Exp Morphol, 95, 131-145.
27. Woodring PJ, Litwack ED, O'Leary DD, et al. (2002): Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J Cell Biol, 156, 879-892.
28. Yaba A, Kayisli UA, Johnson J, et al. (2011): The Abelson tyrosine kinase (c-Abl) expression on the mouse uterus and placenta during gestational period. J Mol Histol, 42, 91-96

Year 2019, Volume: 66 Issue: 1, 89 - 93, 31.12.2018

Duygu Mutluay , Hakan Öner

Abstract

References

1. Abelson HT, Rabstein LS (1970): Lymphosarcoma: virusinduced thymic-independent disease in mice. Cancer Res, 30, 2213-2222.
2. Ahmad K, Naz RK (1994): Protein phosphorylation pattern and role of products of c-erbB-1 and c-abl protooncogenes in murine preimplantation embryonic development. Am J Reprod Immunol, 32, 226–237.
3. Ben-Neriah Y, Daley GQ, Mes-Masson AM, et al. (1986): The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science, 233, 212– 214.
4. Bradley WD, Koleske AJ (2009): Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts. J. Cell Sci, 122, 3441–3454.
5. Brunet S, Maro B (2005): Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction, 130, 801-811.
6. Colicelli J (2011): ABL tyrosine kinases: evolution of function, regulation, and specificity. Sci Signal, 4(188):er4.
7. Diaz H, Esponda P (2004): Ageing-induced changes in the cortical granules of mouse eggs. Zygote, 12, 95–103.
8. Goff SP, Gilboa E, Witte ON, et al. (1980): Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell, 22, 777–785.
9. Gonzalez C (2007): Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nature Rev Genet, 8, 462–472.
10. Greuber EK, Smith-Pearson P, Wang J, et al. (2013): Role of ABL family kinases in cancer: from leukaemia to solid tumours. Nat Rev Cancer, 13, 559-571.
11. Hantschel O, Superti-Furga G (2004): Regulation of the c Abl and Bcr-Abl tyrosine kinases. Nature Rev Mol Cell Biol, 5, 33–44.
12. Hernandez SE, Krishnaswami M, Miller AL, et al. (2004): How do Abl family kinases regulate cell shape and movement? Trends Cell Biol, 4, 36-44.
13. Iwaoki Y, Matsuda H, Mutter GL, et al. (1993): Differential expression of the proto-oncogenes c-abl and cmos in developing mouse germ cells. Exp Cell Res, 206, 212–219.
14. Li B, Boast S, de los Santos K, et al. (2000): Mice deficient in Abl are osteoporotic and have defects in osteoblast maturation. Nature Genet, 24, 304–308.
15. Ma SF, Liu XY, Miao DQ, et al. (2005): Parthenogenetic activation of mouse oocytes by strontium chloride: a search for the best conditions. Theriogenology, 64, 1142-1157.
16. Maro B, Verlhac MH (2002): Polar body formation: new rules for asymmetric divisions. Nat Cell Biol, 4, E281-3.
17. Matsumura S, Hamasaki M, Yamamoto T, et al. (2012): ABL1 regulates spindle orientation in adherent cells and mammalian skin. Nat Commun, 3, 626.
18. Moore KL, Kinsey WH (1994): Identification of an ablrelated protein tyrosine kinase in the cortex of the sea urchin egg: possible role at fertilization. Dev Biol, 164, 444–455.
19. Moore KL, Kinsey WH (1995): Effects of protein tyrosine kinase inhibitors on egg activation and fertilizationdependent protein tyrosine kinase activity. Dev Biol, 168, 1-10.
20. Mutluay D (2016): Distribution of primitive endoderm and epiblast lineage specific factors in late stage blastocysts. Slov Vet Res, 53, 211-217.
21. Mutluay D, Oner H (2017): The Abelson tyrosine kinase (c-Abl) Localization in Preimplantation Mouse Development. Rom J Morphol Embryol, 58, 1385-1391.
22. Nagy A, Gertsenstein M, Vintersten K, et al. (2003): Collection of zygotes and removal of cumulus cells with hyluronidase. 139-142. In: Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
23. Tybulewicz VL, Crawford CE, Jackson PK, et al. (1991): Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell, 65, 1153–1163.
24. Walker G, Burgess D, Kinsey WH (1996): Fertilization promotes selective association of the Abl [correction of AbI] kinase with the egg cytoskeleton. Eur J Cell Biol, 70, 165- 171.
25. Wang JY (2014): The capable ABL: what is its biological function? Mol Cell Biol, 34, 1188-1197.
26. Webb M, Howlett SK, Maro B (1986): Parthenogenesis and cytoskeletal organization in ageing mouse eggs. J Embryol Exp Morphol, 95, 131-145.
27. Woodring PJ, Litwack ED, O'Leary DD, et al. (2002): Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J Cell Biol, 156, 879-892.
28. Yaba A, Kayisli UA, Johnson J, et al. (2011): The Abelson tyrosine kinase (c-Abl) expression on the mouse uterus and placenta during gestational period. J Mol Histol, 42, 91-96

There are 28 citations in total.

Details

Primary Language	English
Journal Section	Research Article
Authors	Duygu Mutluay Hakan Öner
Publication Date	December 31, 2018
Published in Issue	Year 2019Volume: 66 Issue: 1

Cite

APA	Mutluay, D., & Öner, H. (2018). Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 66(1), 89-93.
AMA	Mutluay D, Öner H. Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro. Ankara Univ Vet Fak Derg. December 2018;66(1):89-93.
Chicago	Mutluay, Duygu, and Hakan Öner. “Relationships Between Abelson Tyrosine Kinase (c-Abl) and Spindle During Meiotic Division in Mouse Oocyte in Vitro”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66, no. 1 (December 2018): 89-93.
EndNote	Mutluay D, Öner H (December 1, 2018) Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66 1 89–93.
IEEE	D. Mutluay and H. Öner, “Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro”, Ankara Univ Vet Fak Derg, vol. 66, no. 1, pp. 89–93, 2018.
ISNAD	Mutluay, Duygu - Öner, Hakan. “Relationships Between Abelson Tyrosine Kinase (c-Abl) and Spindle During Meiotic Division in Mouse Oocyte in Vitro”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66/1 (December 2018), 89-93.
JAMA	Mutluay D, Öner H. Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro. Ankara Univ Vet Fak Derg. 2018;66:89–93.
MLA	Mutluay, Duygu and Hakan Öner. “Relationships Between Abelson Tyrosine Kinase (c-Abl) and Spindle During Meiotic Division in Mouse Oocyte in Vitro”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 66, no. 1, 2018, pp. 89-93.
Vancouver	Mutluay D, Öner H. Relationships between Abelson tyrosine kinase (c-abl) and spindle during meiotic division in mouse oocyte in vitro. Ankara Univ Vet Fak Derg. 2018;66(1):89-93.

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