Complement factors are secreted in human follicular fluid by granulosa cells and are possible oocyte maturation factors

Yoo, Seung‐Min; Bolbot, T.; Koulova, Anna; Sneeringer, R.M.; Humm, Kathrin; Dagon, Yossi; Usheva, Anny

doi:10.1111/j.1447-0756.2012.01985.x

Cited by 27 publications

(18 citation statements)

References 22 publications

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“…Complement C8 alpha chain was found in higher abundance (1.4-fold) in pre-hCG FF. The role of the complement factors in follicle maturation is unclear, though it has been postulated that they are possible oocyte maturation factors [ 74 ]. Another complement factor, C3, was differentially expressed in women with severe ovarian hyperstimulation syndrome [ 69 ].…”

Section: Resultsmentioning

confidence: 99%

Proteomic analysis of human follicular fluid from fertile women

Zamah

Hassis²,

Albertolle³

et al. 2015

Clin Proteom

113

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BackgroundFollicular fluid is a unique biological fluid in which the critical events of oocyte and follicular maturation and somatic cell-germ cell communication occur. Because of the intimate proximity of follicular fluid to the maturing oocyte, this fluid provides a unique window into the processes occurring during follicular maturation. A thorough identification of the specific components within follicular fluid may provide a better understanding of intrafollicular signaling, as well as reveal potential biomarkers of oocyte health for women undergoing assisted reproductive treatment. In this study, we used high and low pH HPLC peptide separations followed by mass spectrometry to perform a comprehensive proteomic analysis of human follicular fluid from healthy ovum donors. Next, using samples from a second set of patients, an isobaric mass tagging strategy for quantitative analysis was used to identify proteins with altered abundances after hCG treatment.ResultsA total of 742 follicular fluid proteins were identified in healthy ovum donors, including 413 that have not been previously reported. The proteins belong to diverse functional groups including insulin growth factor and insulin growth factor binding protein families, growth factor and related proteins, receptor signaling, defense/immunity, anti-apoptotic proteins, matrix metalloprotease related proteins, and complement activity. In a quantitative analysis, follicular fluid samples from age-matched women undergoing in vitro fertilization oocyte retrieval were compared and 17 follicular fluid proteins were found at significantly altered levels (p < 0.05) between pre-hCG and post-hCG samples. These proteins belong to a variety of functional processes, including protease inhibition, inflammation, and cell adhesion.ConclusionsThis database of FF proteins significantly extends the known protein components present during the peri-ovulatory period and provides a useful basis for future studies comparing follicular fluid proteomes in various fertility, disease, and environmental exposure conditions. We identified 17 differentially expressed proteins after hCG treatment and together these data showed the feasibility for defining biomarkers that illuminate how the ovarian follicle microenvironment is altered in various infertility-related conditions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12014-015-9077-6) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Proteomic analysis of human follicular fluid from fertile women

Zamah

Hassis²,

Albertolle³

et al. 2015

Clin Proteom

113

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“…This implies that the FF component that compromises sperm viability has a size between 30 and 100 kDa, but can be neutralized by hea inactivation or charcoal treatment. Heat inactivation causes the breakdown of tertiary and quaternary protein structures and could, for example, neutralize complement factors that might be activated under in vitro conditions due to exposure to air (Yoo et al 2013). Charcoal treatment extracts the lipid fraction including steroids and lipoproteins (Cheng et al 1998).…”

Section: Discussionmentioning

confidence: 99%

An alkaline follicular fluid fraction induces capacitation and limited release of oviduct epithelium-bound stallion sperm

et al. 2015

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Induction of hyperactivated motility is considered essential for triggering the release of oviduct-bound mammalian spermatozoa in preparation for fertilization. In this study, oviduct-bound stallion spermatozoa were exposed for 2 h to: i) pre-ovulatory and ii) post-ovulatory oviductal fluid; iii) 100% and iv) 10% follicular fluid (FF); v) cumulus cells, vi) mature equine oocytes, vii) capacitating and viii) non-capacitating medium. None of these triggered sperm release or hyperactivated motility. Interestingly, native FF was detrimental to sperm viability, an effect that was negated by heat inactivation, charcoal treatment and 30 kDa filtration alone or in combination. Moreover, sperm suspensions exposed to treated FF at pH 7.9 but not pH 7.4 showed Ca 2C -dependent hypermotility. Fluo-4 AM staining of sperm showed elevated cytoplasmic Ca 2C in hyperactivated stallion spermatozoa exposed to treated FF at pH 7.9 compared to a modest response in defined capacitating conditions at pH 7.9 and no response in treated FF at pH 7.4. Moreover, 1 h incubation in alkaline, treated FF induced protein tyrosine phosphorylation in 20% of spermatozoa. None of the conditions tested induced widespread release of sperm pre-bound to oviduct epithelium. However, the hyperactivating conditions did induce release of 70-120 spermatozoa per oviduct explant, of which 48% showed protein tyrosine phosphorylation and all were acrosome-intact, but capable of acrosomal exocytosis in response to calcium ionophore. We conclude that, in the presence of elevated pH and extracellular Ca 2C , a heat-resistant, hydrophilic, !30 kDa component of FF can trigger protein tyrosine phosphorylation, elevated cytoplasmic Ca 2C and hyperactivated motility in stallion sperm, but infrequent release of sperm pre-bound to oviduct epithelium. Reproduction (2015) 150 193-208

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“…Proteins of the complement system are widely expressed in the female reproductive tract and were already detected in cumulus cells and oocytes 36,44,45 . The complement system was already characterized as an important constituent of the follicular fluid 34,35,37,46 . RNA analysis of granulosa cells revealed that complement factors are actively produced by these somatic cells 37 .…”

Section: Discussionmentioning

confidence: 99%

“…The complement system was already characterized as an important constituent of the follicular fluid 34,35,37,46 . RNA analysis of granulosa cells revealed that complement factors are actively produced by these somatic cells 37 . The accumulation of C3 in maturation medium in this study supports this hypothesis.…”

Section: Discussionmentioning

confidence: 99%

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The bovine cumulus proteome is influenced by maturation condition and maturational competence of the oocyte

Walter

Monthoux

Fortes

et al. 2020

Sci Rep

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In vitro maturation (IVM) of oocytes has still a negative impact on the developmental competence of oocytes. Therefore, this study analysed the cumulus proteome of individual cumulus-oocyte complexes (COCs) with and without maturational competence, matured under in vivo or in vitro conditions (n = 5 per group). A novel, ultrasensitive mass spectrometry (MS) based protein profiling approach, using label-free quantification, was applied. The detected cumulus proteome included 2226 quantifiable proteins and was highly influenced by the maturation condition (479 differentially expressed proteins) as well as maturational competence of the corresponding oocyte (424 differentially expressed proteins). Enrichment analysis showed an overrepresentation of the complement and coagulation cascades (CCC), ECM-receptor interaction and steroid biosynthesis in cumulus of COCs that matured successfully under in vivo conditions. Verification of the origin of CCC proteins was achieved through detection of C3 secretion into the maturation medium, with significantly increasing concentrations from 12 (48.4 ng/ ml) to 24 hours (68 ng/ml: p < 0.001). In relation, concentrations in follicular fluid, reflecting the in vivo situation, were >100x higher. In summary, this study identified important pathways that are impaired in IVM cumulus, as well as potential markers of the maturational competence of oocytes.

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Complement factors are secreted in human follicular fluid by granulosa cells and are possible oocyte maturation factors

Cited by 27 publications

References 22 publications

Proteomic analysis of human follicular fluid from fertile women

Proteomic analysis of human follicular fluid from fertile women

An alkaline follicular fluid fraction induces capacitation and limited release of oviduct epithelium-bound stallion sperm

The bovine cumulus proteome is influenced by maturation condition and maturational competence of the oocyte

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