Polysialylation takes place in granulosa cells during apoptotic processes of atretic tertiary follicles

FEBS Journal

Volumn 282, Issue 23, 2015, Pages 4595-4606

  Kaese, Miriam ^a   Galuska, Christina E ^a   Simon, Peter ^a   Braun, Beate C ^b   Cabrera Fuentes, Hector A ^a   Middendorff, Ralf ^a   Wehrend, Axel ^a   Jewgenow, Katarina ^b   Galuska, Sebastian P ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

Author keywords

apoptosis; folliculogenesis; granulosa cells; NCAM; polysialic acid

Indexed keywords

LUTEINIZING HORMONE; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE 140; POLYSIALIC ACID; UNCLASSIFIED DRUG; SIALIC ACID DERIVATIVE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; DOMESTIC CAT; FEMALE; GRANULOSA CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORMONAL REGULATION; IMMUNOHISTOCHEMISTRY; NONHUMAN; OVARY FOLLICLE ATRESIA; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIALYLATION; WESTERN BLOTTING; ANIMAL; CAT; CELL CULTURE; CYTOLOGY; METABOLISM; OVARY FOLLICLE;

ANIMALS; APOPTOSIS; CATS; CELLS, CULTURED; FEMALE; FOLLICULAR ATRESIA; GRANULOSA CELLS; OVARIAN FOLLICLE; SIALIC ACIDS;

EID: 84969316696     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13519     Document Type: Article

References (50)

1. Schauer R, (2004) Sialic acids: fascinating sugars in higher animals and man. Zoology (Jena) 107, 49-64.
2. Schauer R, (2009) Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol 19, 507-514.
3. Hildebrandt H, Mühlenhoff M, &, Gerardy-Schahn R, (2008) Polysialylation of NCAM. Adv Exp Med Biol 663, 95-109.
4. Troy FA II, (1992) Polysialylation: from bacteria to brains. Glycobiology 2, 5-23.
5. Colley KJ, (2010) Structural basis for the polysialylation of the neural cell adhesion molecule. Adv Exp Med Biol 663, 111-126.
6. Mühlenhoff M, Rollenhagen M, Werneburg S, Gerardy-Schahn R, &, Hildebrandt H, (2013) Polysialic acid: versatile modification of NCAM, SynCAM 1 and neuropilin-2. Neurochem Res 38, 1134-1143.
7. Colley KJ, Kitajima K, &, Sato C, (2014) Polysialic acid: biosynthesis, novel functions and applications. Crit Rev Biochem Mol Biol 49, 498-532.
8. Galuska SP, Oltmann-Norden I, Geyer H, Weinhold B, Kuchelmeister K, Hildebrandt H, Gerardy-Schahn R, Geyer R, &, Mühlenhoff M, (2006) Polysialic acid profiles of mice expressing variant allelic combinations of the polysialyltransferases ST8SiaII and ST8SiaIV. J Biol Chem 281, 31605-31615.
9. Galuska SP, Geyer R, Gerardy-Schahn R, Mühlenhoff M, &, Geyer H, (2008) Enzyme-dependent variations in the polysialylation of the neural cell adhesion molecule (NCAM) in vivo. J Biol Chem 283, 17-28.
10. Kleene R, &, Schachner M, (2004) Glycans and neural cell interactions. Nat Rev Neurosci 5, 195-208.
11. Rutishauser U, (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 9, 26-35.
12. Puchkov D, Leshchyns'ka I, Nikonenko AG, Schachner M, &, Sytnyk V, (2011) NCAM/spectrin complex disassembly results in PSD perforation and postsynaptic endocytic zone formation. Cereb Cortex 21, 2217-2232.
13. Schnaar RL, Gerardy-Schahn R, &, Hildebrandt H, (2014) Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev 94, 461-518.
14. Moller CJ, Byskov AG, Roth J, Celis JE, &, Bock E, (1991) NCAM in developing mouse gonads and ducts. Anat Embryol 184, 541-548.
15. Bristol-Gould S, &, Woodruff TK, (2006) Folliculogenesis in the domestic cat (Felis catus). Theriogenology 66, 5-13.
16. Li R, &, Albertini DF, (2013) The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol 14, 141-152.
17. Fair T, Hulshof SC, Hyttel P, Greve T, &, Boland M, (1997) Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Mol Reprod Dev 46, 208-215.
18. Asselin E, Xiao CW, Wang YF, &, Tsang BK, (2000) Mammalian follicular development and atresia: role of apoptosis. Neurosignals 9, 87-95.
19. Jewgenow K, Wood TC, &, Wildt DE, (1997) DNA degradation in mural granulosa cells of non- and slightly atretic follicles of fresh and cold-stored domestic cat ovaries. Mol Reprod Dev 48, 350-355.
20. Yang MY, &, Rajamahendran R, (2000) Involvement of apoptosis in the atresia of nonovulatory dominant follicle during the bovine estrous cycle. Biol Reprod 63, 1313-1321.
21. Asahara S, Sato A, Aljonaid AA, &, Maruo T, (2003) Thyroid hormone synergizes with follicle stimulating hormone to inhibit apoptosis in porcine granulosa cells selectively from small follicles. Kobe J Med Sci 49, 107-116.
22. Concannon P, Hodgson B, &, Lein D, (1980) Reflex LH release in estrous cats following single and multiple copulations. Biol Reprod 23, 111-117.
23. Galuska SP, Rollenhagen M, Kaup M, Eggers K, Oltmann-Norden I, Schiff M, Hartmann M, Weinhold B, Hildebrandt H, Geyer R, et al,. (2010) Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc Natl Acad Sci USA 107, 10250-10255.
24. Simon P, Bäumner S, Busch O, Röhrich R, Kaese M, Richterich P, Wehrend A, Müller K, Gerardy-Schahn R, Mühlenhoff M, et al,. (2013) Polysialic acid is present in mammalian semen as a post-translational modification of the neural cell adhesion molecule NCAM and the polysialyltransferase ST8SiaII. J Biol Chem 288, 18825-18833.
25. Buttner B, Kannicht C, Reutter W, &, Horstkorte R, (2003) The neural cell adhesion molecule is associated with major components of the cytoskeleton. Biochem Biophys Res Commun 310, 967-971.
26. Pollerberg GE, Burridge K, Krebs KE, Goodman SR, &, Schachner M, (1987) The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res 250, 227-236.
27. Sasson R, &, Amsterdam A, (2002) Stimulation of apoptosis in human granulosa cells from in vitro fertilization patients and its prevention by dexamethasone: involvement of cell contact and bcl-2 expression. J Clin Endocrinol Metab 87, 3441-3451.
28. Ulm C, Saffarzadeh M, Mahavadi P, Müller S, Prem G, Saboor F, Simon P, Middendorff R, Geyer H, Henneke I, et al,. (2013) Soluble polysialylated NCAM: a novel player of the innate immune system in the lung. Cell Mol Life Sci 70, 3695-3708.
29. Stamatos NM, Zhang L, Jokilammi A, Finne J, Chen WH, El-Maarouf A, Cross AS, &, Hankey KG, (2014) Changes in polysialic acid expression on myeloid cells during differentiation and recruitment to sites of inflammation: role in phagocytosis. Glycobiology 24, 864-879.
30. Hänsch M, Simon P, Schön J, Kaese M, Braun BC, Jewgenow K, Göritz F, Küpper J, Ahmadvand N, Geyer R, et al,. (2014) Polysialylation of NCAM correlates with onset and termination of seasonal spermatogenesis in roe deer. Glycobiology 24, 488-493.
31. Makrigiannakis A, Coukos G, Christofidou-Solomidou M, Gour BJ, Radice GL, Blaschuk O, &, Coutifaris C, (1999) N-cadherin-mediated human granulosa cell adhesion prevents apoptosis: a role in follicular atresia and luteolysis? Am J Pathol 154, 1391-1406.
32. Peluso JJ, Pappalardo A, &, Fernandez G, (2001) E-cadherin-mediated cell contact prevents apoptosis of spontaneously immortalized granulosa cells by regulating Akt kinase activity. Biol Reprod 64, 1183-1190.
33. Johnson CP, Fujimoto I, Rutishauser U, &, Leckband DE, (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 280, 137-145.
34. Oltmann-Norden I, Galuska SP, Hildebrandt H, Geyer R, Gerardy-Schahn R, Geyer H, &, Mühlenhoff M, (2008) Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development. J Biol Chem 283, 1463-1471.
35. Sytnyk V, Leshchyns'ka I, Nikonenko AG, &, Schachner M, (2006) NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. J Cell Biol 174, 1071-1085.
36. Seidenfaden R, Krauter A, Schertzinger F, Gerardy-Schahn R, &, Hildebrandt H, (2003) Polysialic acid directs tumor cell growth by controlling heterophilic neural cell adhesion molecule interactions. Mol Cell Biol 23, 5908-5918.
37. Rockle I, Seidenfaden R, Weinhold B, Muhlenhoff M, Gerardy-Schahn R, &, Hildebrandt H, (2008) Polysialic acid controls NCAM-induced differentiation of neuronal precursors into calretinin-positive olfactory bulb interneurons. Dev Neurobiol 68, 1170-1184.
38. Xia Z, Dickens M, Raingeaud J, Davis RJ, &, Greenberg ME, (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
39. Cheung EC, &, Slack RS, (2004) Emerging role for ERK as a key regulator of neuronal apoptosis. Sci STKE 2004, PE45.
40. Gebauer G, Peter AT, Onesime D, &, Dhanasekaran N, (1999) Apoptosis of ovarian granulosa cells: correlation with the reduced activity of ERK-signaling module. J Cell Biochem 75, 547-554.
41. Peter AT, &, Dhanasekaran N, (2003) Apoptosis of granulosa cells: a review on the role of MAPK-signalling modules. Reprod Domest Anim 38, 209-213.
42. Frosch M, Gorgen I, Boulnois GJ, Timmis KN, &, Bitter-Suermann D, (1985) NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc Natl Acad Sci USA 82, 1194-1198.
43. Stummeyer K, Dickmanns A, Mühlenhoff M, Gerardy-Schahn R, &, Ficner R, (2005) Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12, 90-96.
44. Jewgenow K, &, Rudolph M, (2001) Timing and location of zona pellucida synthesis during oogenesis in domestic cats-an ultrastructural immunohistological investigation. J Reprod Fertil Suppl 57, 23-29.
45. Ringleb J, Rohleder M, &, Jewgenow K, (2004) Impact of feline zona pellucida glycoprotein B-derived synthetic peptides on in vitro fertilization of cat oocytes. Reproduction 127, 179-186.
46. Jolly PD, Smith PR, Heath DA, Hudson NL, Lun S, Still LA, Watts CH, &, McNatty KP, (1997) Morphological evidence of apoptosis and the prevalence of apoptotic versus mitotic cells in the membrana granulosa of ovarian follicles during spontaneous and induced atresia in ewes. Biol Reprod 56, 837-846.
47. Rodgers RJ, &, Irving-Rodgers HF, (2010) Morphological classification of bovine ovarian follicles. Reproduction 139, 309-318.
48. Wood TC, &, Wildt DE, (1997) Effect of the quality of the cumulus-oocyte complex in the domestic cat on the ability of oocytes to mature, fertilize and develop into blastocysts in vitro. J Reprod Fertil 110, 355-360.
49. Simsekyilmaz S, Cabrera-Fuentes HA, Meiler S, Kostin S, Baumer Y, Liehn EA, Weber C, Boisvert WA, Preissner KT, &, Zernecke A, (2014a) Response to letter regarding article 'Role of extracellular RNA in atherosclerotic plaque formation in mice'. Circulation 130, e144-e145.
50. Simsekyilmaz S, Cabrera-Fuentes HA, Meiler S, Kostin S, Baumer Y, Liehn EA, Weber C, Boisvert WA, Preissner KT, &, Zernecke A, (2014b) Role of extracellular RNA in atherosclerotic plaque formation in mice. Circulation 129, 598-606.