Phosphoinositol Turnover Pathway

DOES INTRACELLULAR CALCIUM PLAY A ROLE IN THE INDUCTION OF MEIOSIS?

The presence and importance of a hormone-induced increase in [Ca++]i and the importance of any such increase in the induction of meiotic cell division in the Xenopus oocyte has been the subject of much debate. Although some have reported elevation of [Ca++]i, Robinson (1985) and Cork et al. (1987) [SEE REFERENCES LISTED BELOW] concluded that there is no increase in [Ca++]i after progesterone addition to Xenopus oocytes. A similar conclusion was stated for the involvement of [Ca++]i in germinal vesicle breakdown in the mouse oocyte (Tombes et al., 1992).

Consistent with this belief is that acetylcholine addition to oocytes increases IP3 and [Ca++]i yet there is no induction of meiosis (Gelerstein et al., 1988). Short or long term release of [Ca++]i by various inositol phosphate derivatives was able to speed hormone-induced meiosis yet the derivatives were unable to induce meiosis (Stith and Maller, 1987; Stith and Proctor, 1989). Expression of a constitutively active (but not the wild type) calcium/calmodulin-dependent protein kinase is able to induce migration of the germinal vesicle but not germinal vesicle breakdown (Waldmann et al., 1990).

There is much evidence supporting a hormone-stimulated elevation of [Ca++]i and that this increase plays a role in the induction of meiosis. Calcium ionophores combined with elevated external [Ca++], agents that alter calcium fluxes or displace calcium, and microinjection of calcium-calmodulin all induce meiosis (see summaries in Cicirelli and Smith, 1987; Duesbery and Masui, 1996a). Progesterone addition to oocytes is associated with changes in 45Ca++ fluxes that may be a result of elevated [Ca++]i (O'Connor et al., 1977; Duesbery and Masui, 1996a). Morrill et al. (1984) suggested that progesterone increases [Ca++]i or "membrane calcium" to induce the increase in intracellular pH found after hormone addition to Rana pipiens. Both progesterone and insulin increase IP3 mass (Stith et al., 1992), myo-[3H]inositol incorporation into polyphosphoinositides (Carrasco et al., 1990) and 32P04 incorporation into major phospholipids including phosphatidylinositol (Stith et al., 1992). Microinjection of a monoclonal antibody to phosphatidylinositol 4,5-phosphate (the precursor of IP3) (Han and Lee, 1995) or reduction of the number of IP3 receptors in Xenopus oocytes (Kobrinsky et al., 1995) inhibits induction of meiosis by progesterone. As found by our lab (Smart et al., 1994) and others (Han and Lee, 1995; Duesbery and Masui, 1995a), calcium chelators or heparin inhibit induction of meiosis by progesterone. We report similar findings for the induction of meiosis by insulin.

The inability to record an increase in [Ca++]i during induction of meiosis is surprising in light of the association between elevated [Ca++]i and mitosis (Tombes et al., 1992; Lu and Means, 1993; Hepler, 1994), that elevated phospholipase C activity is mitogenic (Smith et al., 1989; Valius and Kazlauskas, 1993) and that elevated [Ca++]i stimulates tyrosine phosphorylation of MAP kinase (Franklin et al., 1994; Duesbery and Masui, 1996b). MAP kinase has been implicated as a major activator of cdc2 and meiosis (Haccard et al., 1995). A possible explanation for the inability of elevated [Ca++]i to induce meiosis is that another event is required. Duesbery and Masui (1996a) find that depolymerization of microtubules (which occurs normally during hormone induction of meiosis) coupled with [Ca++]i elevated by ionophore is sufficient to induce meiosis in the Xenopus oocyte (in the presence of physiological external calcium concentrations, ionophore was ineffective).

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