Recombinant human ZP3-induced sperm acrosome reaction: Evidence for the involvement of T- and L-type voltage-gated calcium channels

Omar, José; Hernández-Hernández, Óscar; Chirinos, Mayel; González-González, María Elena; Larrea, Fernando; Almanza, Angélica; Felix, Ricardo; Darszon, Alberto; Treviño, Claudia L.

doi:10.1016/j.bbrc.2010.04.059

Cited by 32 publications

(30 citation statements)

References 24 publications

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“…87,101 E. coli-expressed recombinant human ZP1, ZP3 and ZP4 fail to induce any significant increase in the AR, whereas baculovirusexpressed recombinant ZP1, ZP3 and ZP4 induce dose-dependent increases in the AR. 31,32,52,53,61 These studies suggest that glycosylation of human zona proteins is critical for induction of the AR. Expression of recombinant human ZP3 and ZP4 using a baculovirus expression system in the presence of tunicamycin made available these proteins with reduced N-linked oligosaccharides.…”

Section: Zona-induced Acrosome Reaction Sk Gupta and B Bhandari 102mentioning

confidence: 91%

“…[28][29][30] A role for L-type VOCCs has also been proposed during induction of the AR. 31,32 Inhibition of solubilized ZP-mediated AR induction by 3-quinuclidinyl benzilate (an antagonist of muscarinic receptors), tyrphostin A-48 (a tyrosine kinase inhibitor) and pertussis toxin (an inhibitor of G i protein signalling) suggests that the binding of the ZP to sperm plasma membrane receptors involves several downstream signalling pathways. 28 Spermatozoa maintain an inwardly negative membrane potential and conductance through cation channels, producing a depolarizing current.…”

Section: Signalling Events During Zp-mediated Acrosomal Exocytosismentioning

confidence: 99%

“…58 In hamsters and humans, ZP3 performs the function of primary sperm receptor. 52,53,55,59 Studies employing purified native human ZP3, 60 as well as baculovirus-expressed recombinant ZP3, 32,52,53,61 have shown dose-dependent increases in acrosomal exocytosis. Moreover, human ZP3 expressed in mammalian cells also leads to an increase in the AR.…”

Section: Zp3mentioning

confidence: 99%

“…E. coli-expressed recombinant human ZP4 binds to the anterior head of capacitated acrosome-intact human spermatozoa but does not induce the AR. 53 On the other hand, baculovirus-expressed recombinant human ZP4 not only binds to the anterior head of capacitated acrosome-intact spermatozoa, but also induces a dose-dependent increase in the AR 32,52,53,61 (Table 1). These observations were further confirmed by employing immunoaffinity purified native human ZP4 from solubilized human ZP.…”

Section: Zp4mentioning

confidence: 99%

“…As discussed above, in humans (in addition to ZP3), ZP1 and ZP4 also mediate the induction of the AR. 31,32,52,53,60,61 Using pharmacological inhibitors, subtle differences in the downstream signalling pathways used by the ZP glycoproteins were observed, which are summarized in Table 2. ZP3-mediated induction of the AR in humans is inhibited by pertussis toxin, whereas pertussis toxin does not inhibit ZP1-or ZP4-mediated acrosomal exocytosis, which indicates that ZP1/ZP4 act through a G i protein-independent pathway.…”

Section: Zp4mentioning

confidence: 99%

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Acrosome reaction: relevance of zona pellucida glycoproteins

Gupta

Bhandari²

2010

Asian J Androl

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During mammalian fertilisation, the zona pellucida (ZP) matrix surrounding the oocyte is responsible for the binding of the spermatozoa to the oocyte and induction of the acrosome reaction (AR) in the ZP-bound spermatozoon. The AR is crucial for the penetration of the ZP matrix by spermatozoa. The ZP matrix in mice is composed of three glycoproteins designated ZP1, ZP2 and ZP3, whereas in humans, it is composed of four (ZP1, ZP2, ZP3 and ZP4). ZP3 acts as the putative primary sperm receptor and is responsible for AR induction in mice, whereas in humans (in addition to ZP3), ZP1 and ZP4 also induce the AR. The ability of ZP3 to induce the AR resides in its C-terminal fragment. O-linked glycans are critical for the murine ZP3-mediated AR. However, N-linked glycans of human ZP1, ZP3 and ZP4 have important roles in the induction of the AR. Studies with pharmacological inhibitors showed that the ZP3-induced AR involves the activation of the G i -coupled receptor pathway, whereas ZP1-and ZP4-mediated ARs are independent of this pathway. The ZP3-induced AR involves the activation of T-type voltage-operated calcium channels (VOCCs), whereas ZP1-and ZP4-induced ARs involve both T-and L-type VOCCs. To conclude, in mice, ZP3 is primarily responsible for the binding of capacitated spermatozoa to the ZP matrix and induction of the AR, whereas in humans (in addition to ZP3), ZP1 and ZP4 also participate in these stages of fertilisation. Keywords: acrosome reaction; fertilisation; oocyte; signalling pathways; spermatozoa; zona pellucida glycoproteins INTRODUCTION Mammalian fertilisation is a highly synchronized process that involves a complex series of interactions between the spermatozoon and the egg, culminating in their unison. The initial steps in fertilisation involves the binding of the spermatozoon to the zona pellucida (ZP) matrix surrounding the egg, followed by induction of the acrosome reaction (AR) in the zona-bound spermatozoon, a pre-requisite for penetration of the ZP matrix by the spermatozoon. The spermatozoon acrosome is a Golgi-derived organelle that forms a cap over the anterior two-thirds of its nucleus. The AR involves the fusion of the sperm membrane with the outer acrosomal membrane, resulting in release of the acrosomal contents and exposure of the inner acrosomal membrane on the anterior head of the spermatozoon. Various physiological agents, such as progesterone, serum albumin, follicular fluid, hormones (including biogenic amines), hydrolytic enzymes (particularly proteases), hyaluronic acid and ZP glycoproteins, have been implicated in the induction of the AR. [1][2][3] In the present paper, we review the role of the ZP matrix and its constituents in AR induction. Various downstream signalling pathways involved in the ZP glycoprotein-induced AR will also be discussed. On the basis of the current literature and studies from our group, the salient differences in the ZP glycoprotein-mediated induction of the AR in mouse versus human will be highlighted.

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Section: Zona-induced Acrosome Reaction Sk Gupta and B Bhandari 102mentioning

confidence: 91%

Section: Signalling Events During Zp-mediated Acrosomal Exocytosismentioning

confidence: 99%

Section: Zp3mentioning

confidence: 99%

Section: Zp4mentioning

confidence: 99%

Section: Zp4mentioning

confidence: 99%

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Acrosome reaction: relevance of zona pellucida glycoproteins

Gupta

Bhandari²

2010

Asian J Androl

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T-type Ca2+ channels in spermatogenic cells and sperm

Darszon

Hernández‐Cruz

2014

Pflugers Arch - Eur J Physiol

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Cell function is importantly regulated by the intracellular concentration of Ca(2+) ([Ca(2+)]i). Sperm development and function are deeply influenced by [Ca(2+)]i which is modulated amongst other ion transporters by plasma membrane Ca(2+) permeable channels. The presence and role of voltage-dependent Ca(2+) channels (CaV) of the T-type (CaV3) in sperm physiology have become a matter of debate in recent years. Though they are functionally present in later stages of development in spermatogenic cells and testicular sperm and their mRNAs and proteins detected from spermatogenic cells to mature mammalian spermatozoa, their currents have not been recorded in mature spermatozoa. This review critically summarizes the evidence for the involvement of CaV3 channels in sperm development and function.

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Mammalian zona pellucida glycoproteins: structure and function during fertilization

et al. 2012

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Zona pellucida (ZP) is a glycoproteinaceous translucent matrix that surrounds the mammalian oocyte and plays a critical role in the accomplishment of fertilization. In humans, it is composed of 4 glycoproteins designated as ZP1, ZP2, ZP3 and ZP4, whereas mouse ZP is composed of ZP1, ZP2 and ZP3 (Zp4 being a pseudogene). In addition to a variable sequence identity of a given zona protein among various species, human ZP1 and ZP4 are paralogs and mature polypeptide chains share an identity of 47%. Employing either affinity purified native or recombinant human zona proteins, it has been demonstrated that ZP1, ZP3 and ZP4 bind to the capacitated human spermatozoa and induce an acrosome reaction, whereas in mice, ZP3 acts as the putative primary sperm receptor. Human ZP2 only binds to acrosome-reacted spermatozoa and thus may be acting as a secondary sperm receptor. In contrast to O-linked glycans of ZP3 in mice, N-linked glycans of human ZP3 and ZP4 are more relevant for induction of the acrosome reaction. Recent studies suggest that Sialyl-Lewis(x) sequence present on both N- and O-glycans of human ZP play an important role in human sperm-egg binding. There are subtle differences in the downstream signaling events associated with ZP3 versus ZP1/ZP4-mediated induction of the acrosome reaction. For example, ZP3 but not ZP1/ZP4-mediated induction of the acrosome reaction is dependent on the activation of the Gi protein-coupled receptor. Thus, various studies suggest that, in contrast to mice, in humans more than one zona protein binds to spermatozoa and induces an acrosome reaction.

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Recombinant human ZP3-induced sperm acrosome reaction: Evidence for the involvement of T- and L-type voltage-gated calcium channels

Cited by 32 publications

References 24 publications

Acrosome reaction: relevance of zona pellucida glycoproteins

Acrosome reaction: relevance of zona pellucida glycoproteins

T-type Ca2+ channels in spermatogenic cells and sperm

Mammalian zona pellucida glycoproteins: structure and function during fertilization

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