Expression and functional activity of PACAP and its receptors on cumulus cells: Effects on oocyte maturation

Molecular and Cellular Endocrinology

Volumn 375, Issue 1-2, 2013, Pages 79-88

  Barberi, Marzia ^a   Di Paolo, Virginia ^a   Latini, Stefania ^a   Guglielmo, Maria Cristina ^a,c   Cecconi, Sandra ^b   Canipari, Rita ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF L'AQUILA   (Italy)

^c Biogenesi Reproductive Medicine Centre   (Italy)

Author keywords

Apoptosis; Cumulus expansion; Oocyte maturation; PACAP

Indexed keywords

CHORIONIC GONADOTROPIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1; PHOSPHOLIPASE C;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL EXPANSION; CELL ISOLATION; CELL MATURATION; CONTROLLED STUDY; CUMULUS CELL; DENSITOMETRY; ENZYME SPECIFICITY; FEMALE; FERTILIZATION; GERMINAL VESICLE; MOUSE; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OVULATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANIMALS; APOPTOSIS; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; CHORIONIC GONADOTROPIN; CUMULUS CELLS; CYTOPLASM; EPIDERMAL GROWTH FACTOR; FEMALE; FERTILIZATION IN VITRO; FOLLICLE STIMULATING HORMONE; GLYCOPROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; OOCYTES; OVULATION; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE, TYPE II; RNA, MESSENGER; SPERM HEAD;

EID: 84878937582     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.05.006     Document Type: Article

References (46)

1. Abbott A.L., Fissore R.A., Ducibella T. Incompetence of preovulatory mouse oocytes to undergo cortical granule exocytosis following induced calcium oscillations. Dev. Biol. 1999, 207:38-48.
2. Apa R., Lanzone A., Miceli F., Mastrandrea M., Caruso A., Mancuso S., Canipari R. Growth hormone induces in vitro maturation of follicle- and cumulus-enclosed rat oocytes. Mol. Cell. Endocrinol. 1994, 106:207-212.
3. Apa R., Lanzone A., Miceli F., Mastrandrea M., Macchione E., Caruso A., Mancuso S., Canipari R. Growth hormone-releasing factor stimulates meiotic maturation in follicle- and cumulus-enclosed rat oocyte. Mol. Cell Endocrinol. 1995, 112:195-201.
4. Apa R., Lanzone A., Mastrandrea M., Miceli F., Macchione E., Fulghesu A.M., Caruso A., Canipari R. Effect of pituitary adenylate cyclase-activating peptide on meiotic maturation in follicle-enclosed, cumulus-enclosed, and denuded rat oocytes. Biol. Reprod. 1997, 57:1074-1079.
5. Apa R., Lanzone A., Miceli F., Vaccari S., Macchione E., Stefanini M., Canipari R. Pituitary adenylate cyclase-activating polypeptide modulates plasminogen activator expression in rat granulosa cell. Biol. Reprod. 2002, 66:830-835.
6. Arimura A. Pituitary adenylate cyclase activating polypeptide (PACAP): discovery and current status of research. Regulat. Peptides 1992, 37:287-302.
7. Arimura A. Receptors for pituitary adenylate cyclase-activating polypeptide: comparison with vasoactive intestinal peptide receptors. Trends Endocrinol. Metab. 1992, 3:288-294.
8. Baker, T.G., 1972. Oogenesis and ovulation, pp. 14-45.
9. Barberi M., Muciaccia B., Morelli M.B., Stefanini M., Cecconi S., Canipari R. Expression localisation and functional activity of pituitary adenylate cyclase-activating polypeptide, vasoactive intestinal polypeptide and their receptors in mouse ovary. Reproduction 2007, 134:281-292.
10. Biggers, J.D., Whitten, W.K., Whittingham, D.G. 1971. In: Methods in Mammalian Embryology, Daniel, J.D. (Ed.), (Freeman, San Francisco), pp. 86-116.
11. Billig H., Chun S.Y., Eisenhauer K., Hsueh A.J. Gonadal cell apoptosis: hormone-regulated cell demise. Hum. Reprod. Update. 1996, 2:103-117.
12. Brubel R., Reglodi D., Jambor E., Koppan M., Varnagy A., Biro Z., Kiss P., Gaal V., Matkovits A., Farkas J., Lubics A., Bodis J., Bay C., Veszpremi B., Tamas A., Nemeth J., Mark L. Investigation of pituitary adenylate cyclase activating polypeptide in human gynecological and other biological fluids by using MALDI TOF mass spectrometry. J. Mass Spectrom. 2011, 46:189-194.
13. Canipari R. Oocyte-granulosa cell interactions. Hum. Reprod. Update. 2000, 6:279-289.
14. Canipari R., Epifano O., Siracusa G., Salustri A. Mouse oocytes inhibit plasminogen activator production by ovarian cumulus and granulosa cells. Dev. Biol. 1995, 167:371-378.
15. Canipari R., Cellini V., Cecconi S. The ovary feels fine when paracrine and autocrine networks cooperate with gonadotropins in the regulation of folliculogenesis. Curr. Pharm. Des 2012, 18:245-255.
16. Cecconi S., D'Aurizio R., Colonna R. Role of antral follicle development and cumulus cells on in vitro fertilization of mouse oocytes. J. Reprod. Fertil. 1996, 107:207-214.
17. Cecconi S., Rossi G., Barberi M., Scaldaferri L., Canipari R. Effect of pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal polypeptide on mouse preantral follicle development in vitro. Endocrinology 2004, 145:2071-2079.
18. Chen L., Russell P.T., Larsen W.J. Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol. Reprod. Dev. 1993, 34:87-93.
19. Driancourt M.A., Thuel B. Control of oocyte growth and maturation by follicular cells and molecules present in follicular fluid. A review. Reprod. Nutr. Dev. 1998, 38:345-362.
20. Gottschall P.E., Tatsuno I., Miyata A., Arimura A. Characterization and distribution of binding sites for the hypothalamic peptide, pituitary adenylate cyclase-activating polypeptide. Endocrinology 1990, 127:272-277.
21. Heindel J.J., Sneeden J., Powell C.J., Davis B., Culler M.D. A novel hypothalamic peptide, pituitary adenylate cyclase-activating peptide, regulates the function of rat granulosa cells in vitro. Biol. Reprod. 1996, 54:523-530.
22. Host E., Gabrielsen A., Lindenberg S., Smidt-Jensen S. Apoptosis in human cumulus cells in relation to zona pellucida thickness variation, maturation stage, and cleavage of the corresponding oocyte after intracytoplasmic sperm injection. Fertil. Steril. 2002, 77:511-515.
23. Hsueh A.J., Billig H., Tsafriri A. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr. Rev. 1994, 15:707-724.
24. Izadyar F., Van Tol H.T., Colenbrander B., Bevers M.M. Stimulatory effect of growth hormone on in vitro maturation of bovine oocytes is exerted through cumulus cells and not mediated by IGF-I. Mol. Reprod. Dev. 1997, 47:175-180.
25. Koppan M., Varnagy A., Reglodi D., Brubel R., Nemeth J., Tamas A., Mark L., Bodis J. Correlation between oocyte number and follicular fluid concentration of pituitary adenylate cyclase-activating polypeptide (PACAP) in women after superovulation treatment. J. Mol. Neurosci. 2012, 48:617-622.
26. Lee J., Park H.J., Choi H.S., Kwon H.B., Arimura A., Lee B.J., Choi W.S., Chun S.Y. Gonadotropin stimulation of pituitary adenylate cyclase-activating polypeptide (PACAP) messenger ribonucleic acid in the rat ovary and the role of PACAP as a follicle survival factor. Endocrinology 1999, 140:818-826.
27. Lee K.S., Joo B.S., Na Y.J., Yoon M.S., Choi O.H., Kim W.W. Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J. Assist. Reprod. Genet. 2001, 18:490-498.
28. Luciano A.M., Modina S., Vassena R., Milanesi E., Lauria A., Gandolfi F. Role of intracellular cyclic adenosine 3',5'-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol. Reprod. 2004, 70:465-472.
29. Lutz E.M., Sheward W.J., West K.M., Morrow J.A., Fink G., Harmar A.J. The VIP2 receptor: molecular characterisation of a cDNA encoding a novel receptor for vasoactive intestinal peptide. FEBS Lett. 1993, 334:3-8.
30. Morelli M.B., Barberi M., Gambardella A., Borini A., Cecconi S., Coticchio G., Canipari R. Characterization, expression, and functional activity of pituitary adenylate cyclase-activating polypeptide and its receptors in human granulosa-luteal cells. J. Clin. Endocrinol. Metab. 2008, 93:4924-4932.
31. Nakahara K., Saito H., Saito T., Ito M., Ohta N., Takahashi T., Hiroi M. The incidence of apoptotic bodies in membrana granulosa can predict prognosis of ova from patients participating in in vitro fertilization programs. Fertil. Steril. 1997, 68:312-317.
32. Pantaloni C., Brabet P., Bilanges B., Dumuis A., Houssami S., Spengler D., Bockaert J., Journot L. Alternative splicing in the N-terminal extracellular domain of the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor modulates receptor selectivity and relative potencies of PACAP-27 and PACAP-38 in phospholipase C activation. J. Biol. Chem. 1996, 271:22146-22151.
33. Park J.Y., Su Y.Q., Ariga M., Law E., Jin S.L., Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004, 303:682-684.
34. Park H.J., Choi B.C., Song S.J., Lee D.S., Roh J., Chun S.Y. Luteinizing hormone-stimulated pituitary adenylate cyclase-activating polypeptide system and its role in progesterone production in human luteinized granulosa cells. Endocr. J. 2010, 57:127-134.
35. Reglodi, D., Tamas, A., Koppan, M., Szogyi, D., Welke, L. 2012. Role of PACAP in female fertility and reproduction at gonadal level - recent advances. Front Endocrinol., (Lausanne) vol. 3, p. 155.
36. Ruvolo G., Bosco L., Pane A., Morici G., Cittadini E., Roccheri M.C. Lower apoptosis rate in human cumulus cells after administration of recombinant luteinizing hormone to women undergoing ovarian stimulation for in vitro fertilization procedures. Fertil. Steril. 2007, 87:542-546.
37. Salustri A., Camaioni A., D'Alessandris C. Endocrine and paracrine regulation of cumulus expansion. Zygote 1996, 4:313-315.
38. Sanfins A., Lee G.Y., Plancha C.E., Overstrom E.W., Albertini D.F. Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes. Biol. Reprod. 2003, 69:2059-2067.
39. Sherwood N.M., Krueckl S.L., McRory J.E. The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily. Endocr. Rev. 2000, 21:619-670.
40. Spengler D., Waeber C., Pantaloni C., Holsboer F., Bockaert J., Seeburg P.H., Journot L. Differential signal transduction by five splice variants of the PACAP receptor. Nature 1993, 365:170-175.
41. Tanii I., Aradate T., Matsuda K., Komiya A., Fuse H. PACAP-mediated sperm-cumulus cell interaction promotes fertilization. Reproduction 2011, 141:163-171.
42. Thomas, R.L., Crawford, N.M., Grafer, C.M., Halvorson, L.M., 2012. Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) in the Hypothalamic-Pituitary-Gonadal Axis: A Review of the Literature. Reprod Sci. December 10. [Epub ahead of print].
43. Vaccari S., Latini S., Barberi M., Teti A., Stefanini M., Canipari R. Characterization and expression of different pituitary adenylate cyclase-activating polypeptide/vasoactive intestinal polypeptide receptors in rat ovarian follicles. J. Endocrinol. 2006, 191:287-299.
44. Vanderhyden B.C., Caron P.J., Buccione R., Eppig J.J. Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 1990, 140:307-317.
45. Wang Y., Wong A.O., Ge W. Cloning, regulation of messenger ribonucleic acid expression, and function of a new isoform of pituitary adenylate cyclase-activating polypeptide in the zebrafish ovary. Endocrinology 2003, 144:4799-4810.
46. Zhong Y., Kasson B.G. Pituitary adenylate cyclase-activating polypeptide stimulates steroidogenesis and adenosine 3',5'-monophosphate accumulation in cultured rat granulosa cells. Endocrinology 1994, 135:207-213.