Follicular-fluid proteomics during equine follicle development.
Abstract: The complex composition of the follicular fluid (FF), the intimate proximity to the oocyte, and the continual changes in their composition have a major effect on folliculogenesis and oogenesis. To date, the profiling of FF proteomes during follicle selection, development, and ovulation has not been comprehensively investigated. Therefore, a shotgun proteomics approach and bioinformatics analyses were used to profile the proteomes of equine FF harvested in vivo from follicles at the following development stages: predeviation (18-20 mm), deviation (22-25 mm), postdeviation (26-29 mm), preovulatory (30-35 mm), and impending ovulation. A total of 294 proteins were detected in FF (FDR <1%), corresponding to 65 common proteins and 124, 142, 167, 132, and 142 proteins in the predeviation, deviation, postdeviation, preovulatory, and impending ovulation groups, respectively. The higher expression of properdin and several other proteins belonging to the complement system during the deviation time and ovulation suggested their contribution in the selection of the future dominant follicle and ovulation. Apolipoprotein A-1 and antithrombin-III appeared to be important throughout folliculogenesis. The "complement and coagulation cascades" was the major KEGG pathway across all stages of follicle development. The significant expression of several proteins belonging to the serine-type endopeptidase indicated their likely contribution to follicle and oocyte development. Our data provide an extensive description and functional analyses of the equine FF proteome during follicle selection, development, and ovulation. This information will help improve understanding of the ovarian function and ovulatory dysfunctions and might serve as a reference for future biomarker discovery for oocyte quality assessment.
© 2022 Wiley Periodicals LLC.
Publication Date: 2022-06-27 PubMed ID: 35762042DOI: 10.1002/mrd.23622Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
- Research Support
- U.S. Gov't
- Non-P.H.S.
- Research Support
- N.I.H.
- Extramural
Summary
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The research study investigates the different protein compositions in the follicular fluid (FF) of horses during various stages of follicular development, providing an understanding of their effects on the process of folliculogenesis and oogenesis. The study utilized a shotgun proteomics approach and data processing tools, allowing a thorough understanding of the proteins’ roles in these processes and deriving potential biomarkers for assessing oocyte quality.
Study Design and Methods
- The researchers used a method known as ‘shotgun proteomics’ and various bioinformatics tools to profile the proteins present in equine FF. Shotgun proteomics is a large-scale analysis technique that allows the identification and quantification of proteins in a complex biological sample.
- Equine FF was collected in vivo (in the live animal) from follicles at different stages of development including predeviation, deviation, postdeviation, preovulatory, and impending ovulation.
Findings and Observations
- A total of 294 proteins were identified across all stages of follicular development. These proteins were categorized into 65 common proteins and specific proteins for each stage of development.
- Properdin and other proteins belonging to the complement system showed increased expression during the deviation stage and ovulation, indicating their role in follicle selection and ovulation.
- Apolipoprotein A-1 and antithrombin-III appear to play critical roles throughout folliculogenesis.
- The major KEGG (Kyoto Encyclopedia of Genes and Genomes) pathway identified across all stages was the “complement and coagulation cascades”. This suggests these pathways are crucial for follicle development.
- Higher expression of proteins belonging to the serine-type endopeptidase family suggests their likely involvement in follicle and oocyte development.
Implications and Conclusions
- The findings offer comprehensive insights into the protein composition of equine FF during various stages of follicle development and ovulation.
- Understanding these protein profiles can enhance knowledge of ovarian function and ovulatory dysfunctions.
- This study holds significant potential for future clinical applications, serving as a foundation for biomarker discovery to assess oocyte quality. This could be valuable for fertility studies and treatments in horses and potentially other types of livestock or even human fertility.
Cite This Article
APA
Ishak GM, Feugang JM, Pechanova O, Pechan T, Peterson DG, Willard ST, Ryan PL, Gastal EL.
(2022).
Follicular-fluid proteomics during equine follicle development.
Mol Reprod Dev, 89(7), 298-311.
https://doi.org/10.1002/mrd.23622 Publication
Researcher Affiliations
- Department of Surgery and Obstetrics, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
- Animal Science, School of Agricultural Sciences, Southern Illinois University, Carbondale, Illinois, USA.
- Department of Animal and Dairy Sciences, Mississippi State University, Mississippi State, Mississippi, USA.
- Institute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Mississippi State, Mississippi, USA.
- Institute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Mississippi State, Mississippi, USA.
- Institute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Mississippi State, Mississippi, USA.
- Department of Animal and Dairy Sciences, Mississippi State University, Mississippi State, Mississippi, USA.
- Department of Animal and Dairy Sciences, Mississippi State University, Mississippi State, Mississippi, USA.
- Animal Science, School of Agricultural Sciences, Southern Illinois University, Carbondale, Illinois, USA.
MeSH Terms
- Animals
- Female
- Follicular Fluid / metabolism
- Horses
- Ovarian Follicle / metabolism
- Ovulation
- Proteome / metabolism
- Proteomics
Grant Funding
- P20 GM103476 / NIGMS NIH HHS
References
This article includes 75 references
- Adams G P, Singh J, Baerwald A R. Large animal models for the study of ovarian follicular dynamics in women. Theriogenology 78, 1733-1748.
- Álvarez-Díaz S, Larriba M J, López-Otín C, Muñoz A. Vitamin D: Proteases, protease inhibitors and cancer. Cell Cycle 9, 32-37.
- Ambekar A S, Nirujogi R S, Srikanth S M, Chavan S, Kelkar D S, Hinduja I, Zaveri K, Prasad T K, Harsha H, Pandey A. Proteomic analysis of human follicular fluid: A new perspective towards understanding folliculogenesis. Journal of Proteomics 87, 68-77.
- Baerwald A R. Human antral folliculogenesis: What we have learned from the bovine and equine models. Animal Reproduction 6, 20-29.
- Bashir S T, Baerwald A R, Gastal M O, Pierson R A, Gastal E L. Follicle growth and endocrine dynamics in women with spontaneous luteinized unruptured follicles versus ovulation. Human Reproduction 33, 1130-1140.
- Bianchi L, Gagliardi A, Landi C, Focarelli R, De Leo V, Luddi A, Bini L, Piomboni P. Protein pathways working in human follicular fluid: The future for tailored IVF?. Expert Reviews in Molecular Medicine 18, e9.
- Boots C E, Jungheim E S. Inflammation and human ovarian follicular dynamics. Seminars in Reproductive Medicine 33, 270-275.
- Bunel A, Nivet A L, Blondin P, Vigneault C, Richard F J, Sirard M A. Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes. Reproduction, Fertility, and Development 26, 855-865.
- Campos-Chillon F, Farmerie T A, Bouma G J, Clay C M, Carnevale E M. Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells. Reproduction, Fertility, and Development 27, 925-933.
- Carnevale E M. The mare model for follicular maturation and reproductive aging in the woman. Theriogenology 69, 23-30.
- da Silveira J C, Veeramachaneni D R, Winger Q A, Carnevale E M, Bouma G J. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: A possible new form of cell communication within the ovarian follicle. Biology of Reproduction 86(3), 71.
- de Agostini A I, Dong J-C, de Vantéry Arrighi C, Ramus M-A, Dentand-Quadri I, Thalmann S, Ventura P, Ibecheole V, Monge F, Fischer A-M. Human follicular fluid heparan sulfate contains abundant 3-O-sulfated chains with anticoagulant activity. Journal of Biological Chemistry 283, 28115-28124.
- del Collado M, Andrade G M, Meirelles F V, da Silveira J C, Perecin F. Contributions from the ovarian follicular environment to oocyte function. Animal Reproduction 15, 261-270.
- Duffy D M, Ko C, Jo M, Brannstrom M, Curry T E Jr. Ovulation: Parallels with inflammatory processes. Endocrine Reviews 40, 369-416.
- Dutra G A, Ishak G M, Pechanova O, Pechan T, Peterson D G, Jacob J C F, Willard S T, Ryan P L, Gastal E L, Feugang J M. Seasonal variation in equine follicular fluid proteome. Reproductive Biology and Endocrinology 17, 29.
- Fahiminiya S, Labas V, Roche S, Dacheux J L, Gerard N. Proteomic analysis of mare follicular fluid during late follicle development. Proteome Science 9, 54.
- Ferrazza R A, Garcia H M, Schmidt E S, Carmichael M, Souza F F, Burchmore R, Sartori R, Eckersall P D, Ferreira J P. Quantitative proteomic profiling of bovine follicular fluid during follicle development. Biology of Reproduction 97, 835-849.
- Fortune J E. Ovarian follicular growth and development in mammals. Biology of Reproduction 50, 225-232.
- Fourgeaud L, Boulanger L M. Synapse remodeling, compliments of the complement system. Cell 131, 1034-1036.
- Freitas C, Neto A C, Matos L, Silva E, Ribeiro Â, Silva-Carvalho J L, Almeida H. Follicular fluid redox involvement for ovarian follicle growth. Journal of Ovarian Research 10, 44.
- Fu Q, Huang Y, Wang Z, Chen F, Huang D, Lu Y, Liang X, Zhang M. Proteome profile and quantitative proteomic analysis of buffalo (Bubalusbubalis) follicular fluid during follicle development. International Journal of Molecular Sciences 17, 618.
- Garcia-Guerra A, Wiltbank M C, Battista S E, Kirkpatrick B W, Sartori R. Mechanisms regulating follicle selection in ruminants: Lessons learned from multiple ovulation models. Animal Reproduction 15, 660-679.
- Gastal E L. Recent advances and new concepts on follicle and endocrine dynamics during the equine periovulatory period. Animal Reproduction 6, 144-158.
- Gastal E L, Gastal M O, Bergfelt D R, Ginther O J. Role of diameter differences among follicles in selection of a future dominant follicle in mares. Biology of Reproduction 57, 1320-1327.
- Gastal E L, Gastal M O, Ginther O J. Serrated granulosa and other discrete ultrasound indicators of impending ovulation in mares. Journal of Equine Veterinary Science 26, 67-73.
- Gastal E L, Gastal M O, Ginther O J. Relationships of changes in B-mode echotexture and colour-Doppler signals in the wall of the preovulatory follicle to changes in systemic oestradiol concentrations and the effects of human chorionic gonadotrophin in mares. Reproduction 131, 699-709.
- Gentry P A, Zareie M, Liptrap R M. Fibronectin concentrations correlate with ovarian follicular size and estradiol values in equine follicular fluid. Animal Reproduction Science 45, 91-102.
- Gilchrist R, Ritter L, Armstrong D. Oocyte-somatic cell interactions during follicle development in mammals. Animal Reproduction Science 82, 431-446.
- Ginther O J. The mare: A 1000-pound guinea pig for study of the ovulatory follicular wave in women. Theriogenology 77, 818-828.
- Ginther O J. The theory of follicle selection in cattle. Domestic Animal Endocrinology 57, 85-99.
- Ginther O J, Beg M A, Bergfelt D R, Donadeu F X, Kot K. Follicle selection in monovular species. Biology of Reproduction 65, 638-647.
- Ginther O J, Beg M A, Donadeu F X, Bergfelt D R. Mechanism of follicle deviation in monovular farm species. Animal Reproduction Science 78, 239-257.
- Ginther O J, Beg M A, Gastal E L, Gastal M O, Baerwald A R, Pierson R A. Systemic concentrations of hormones during the development of follicular waves in mares and women: A comparative study. Reproduction 130, 379-388.
- Ginther O J, Gastal E L, Gastal M O, Beg M A. Dynamics of the equine preovulatory follicle and periovulatory hormones: What's new?. Journal of Equine Veterinary Science 28, 454-460.
- Ginther O J, Gastal E L, Gastal M O, Bergfelt D R, Baerwald A R, Pierson R A. Comparative study of the dynamics of follicular waves in mares and women. Biology of Reproduction 71, 1195-1201.
- Gulamali-Majid F, Ackerman S, Veeck L, Acosta A, Pleban P. Kinetic immunonephelometric determination of protein concentrations in follicular fluid. Clinical Chemistry 33, 1185-1189.
- Haag K T, Magalhaes-Padilha D M, Fonseca G R, Wischral A, Gastal M O, King S S, Jones K L, Figueiredo J R, Gastal E L. Quantification, morphology, and viability of equine preantral follicles obtained via the biopsy pick-up method. Theriogenology 79, 599-609.
- Hester K E, Harper M J, Duffy D M. Oral administration of the cyclooxygenase-2 (COX-2) inhibitor meloxicam blocks ovulation in non-human primates when administered to simulate emergency contraception. Human Reproduction 25, 360-367.
- Hiemstra P S. Novel roles of protease inhibitors in infection and inflammation. Biochemical Society Transactions 30, 116-120.
- Ishak G M, Bashir S T, Dutra G A, Gastal G A, Gastal M O, Cavinder C A, Feugang J M, Gastal E L. In vivo antral follicle wall biopsy: A new research technique to study ovarian function at the cellular and molecular levels. Reproductive Biology and Endocrinology 16, 71.
- Jarkovska K, Martinkova J, Liskova L, Halada P, Moos J, Rezabek K, Gadher S J, Kovarova H. Proteome mining of human follicular fluid reveals a crucial role of complement cascade and key biological pathways in women undergoing in vitro fertilization. Journal of Proteome Research 9, 1289-1301.
- Jesam C, Salvatierra A M, Schwartz J L, Croxatto H B. Suppression of follicular rupture with meloxicam, a cyclooxygenase-2 inhibitor: Potential for emergency contraception. Human Reproduction 25, 368-373.
- Junior A R P, van Tilburg M F, Lobo M D, Monteiro-Moreira A C, Moreira R A, Melo C H, Souza-Fabjan J M, Araújo A A, Melo L M, Teixeira D I. Proteomic analysis of follicular fluid from tropically-adapted goats. Animal Reproduction Science 188, 35-44.
- Kemper C, Atkinson J P, Hourcade D E. Properdin: Emerging roles of a pattern-recognition molecule. Annual Review of Immunology 28, 131-155.
- Kemper C, Mitchell L M, Zhang L, Hourcade D E. The complement protein properdin binds apoptotic T cells and promotes complement activation and phagocytosis. Proceedings of the National Academy of Sciences 105, 9023-9028.
- Kenawy H I, Boral I, Bevington A. Complement-coagulation cross-talk: A potential mediator of the physiological activation of complement by low pH. Frontiers in Immunology 6, 215.
- Koskinen E, Kuntsi H, Lindeberg H, Katila T. Predicting ovulation in the mare on the basis of follicular growth and serum oestrone sulphate and progesterone levels. Journal of Veterinary Medicine Series A 36, 299-304.
- Kushnir M M, Naessén T, Wanggren K, Hreinsson J, Rockwood A L, Meikle A W, Bergquist J. Exploratory study of the association of steroid profiles in stimulated ovarian follicular fluid with outcomes of IVF treatment. The Journal of Steroid Biochemistry and Molecular Biology 162, 126-133.
- Lee H-C, Lee S-W, Lee K W, Lee S-W, Cha K-Y, Kim K H, Lee S. Identification of new proteins in follicular fluid from mature human follicles by direct sample rehydration method of two-dimensional polyacrylamide gel electrophoresis. Journal of Korean Medical Science 20, 456-460.
- Lewandowska A E, Macur K, Czaplewska P, Liss J, Łukaszuk K, Ołdziej S. Qualitative and quantitative analysis of proteome and peptidome of human follicular fluid using multiple samples from single donor with LC-MS and SWATH methodology. Journal of Proteome Research 16, 3053-3067.
- Lin G, Oram J F. Apolipoprotein binding to protruding membrane domains during removal of excess cellular cholesterol. Atherosclerosis 149, 359-370.
- Liu J-Q, Li W-X, Zheng J-J, Tian Q-N, Huang J-F, Dai S-X. Gain and loss events in the evolution of the apolipoprotein family in vertebrata. BMC Evolutionary Biology 19, 1-10.
- Mclin V A, Hu C-H, Shah R, Jamrich M. Expression of complement components coincides with early patterning and organogenesis in Xenopus laevis. International Journal of Developmental Biology 52, 1123-1133.
- Michels M A, Volokhina E B, van de Kar N C, van den Heuvel L P. The role of properdin in complement-mediated renal diseases: A new player in complement-inhibiting therapy?. Pediatric Nephrology 34, 1349-1367.
- Muller-Eberhard U. Hemopexin. New England Journal of Medicine 283, 1090-1094.
- Nandi S, Kumar V G, Manjunatha B, Gupta P. Biochemical composition of ovine follicular fluid in relation to follicle size. Development, Growth & Differentiation 49, 61-66.
- Oh J W, Kim S K, Cho K C, Kim M S, Suh C S, Lee J R, Kim K P. Proteomic analysis of human follicular fluid in poor ovarian responders during in vitro fertilization. Proteomics 17, 1600333.
- Oikonomopoulou K, Ricklin D, Ward P A, Lambris J D. Interactions between coagulation and complement-Their role in inflammation. Seminars in immunopathology 34, 151-165.
- Paes V M, de Figueiredo J R, Ryan P L, Willard S T, Feugang J M. Comparative analysis of porcine follicular fluid proteomes of small and large ovarian follicles. Biology 9, 101.
- Paes V M, Liao S F, Figueiredo J R, Willard S T, Ryan P L, Feugang J M. Proteome changes of porcine follicular fluid during follicle development. Journal of Animal Science and Biotechnology 10, 94.
- Palmer E, Driancourt M A. Use of ultrasonic echography in equine gynecology. Theriogenology 13, 203-216.
- Petrucci B, Wolf C, Arlas T, Santos G, Estanislau J, Fiala S, Jobim M, Mattos R. Proteomics of mare follicular fluid during follicle development. Journal of Equine Veterinary Science 1, 115-116.
- Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. Follicular fluid content and oocyte quality: From single biochemical markers to metabolomics. Reproductive Biology and Endocrinology 7, 40.
- Riley-Vargas R C, Lanzendorf S, Atkinson J P. Targeted and restricted complement activation on acrosome-reacted spermatozoa. The Journal of Clinical Investigation 115, 1241-1249.
- Shen X, Liu X, Zhu P, Zhang Y, Wang J, Wang Y, Wang W, Liu J, Li N, Liu F. Proteomic analysis of human follicular fluid associated with successful in vitro fertilization. Reproductive Biology and Endocrinology 15, 58.
- Singh R, Sinclair K D. Metabolomics: Approaches to assessing oocyte and embryo quality. Theriogenology 68, S56-S62.
- Spitzer D, Mitchell L M, Atkinson J P, Hourcade D E. Properdin can initiate complement activation by binding specific target surfaces and providing a platform for de novo convertase assembly. The Journal of Immunology 179, 2600-2608.
- Stevens B, Allen N J, Vazquez L E, Howell G R, Christopherson K S, Nouri N, Micheva K D, Mehalow A K, Huberman A D, Stafford B. The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178.
- Taketani S, Immenschuh S, Go S, Sinclair P R, Stockert R J, Liem H H, Eberhard U M. Hemopexin from four species inhibits the association of heme with cultured hepatoma cells or primary rat hepatocytes exhibiting a small number of species specific hemopexin receptors. Hepatology 27, 808-814.
- van den Hurk R, Zhao J. Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717-1751.
- von Otte S, Paletta J R, Becker S, König S, Fobker M, Greb R R, Kiesel L, Assmann G, Diedrich K, Nofer J-R. Follicular fluid high density lipoprotein-associated sphingosine 1-phosphate is a novel mediator of ovarian angiogenesis. Journal of Biological Chemistry 281, 5398-5405.
- Walter J, Huwiler F, Fortes C, Grossmann J, Roschitzki B, Hu J, Naegeli H, Laczko E, Bleul U. Analysis of the equine “cumulome” reveals major metabolic aberrations after maturation in vitro. BMC Genomics 20, 588.
- Yamada M, Gentry P A. Hemostatic profile of bovine ovarian follicular fluid. Canadian Journal of Physiology and Pharmacology 73, 624-629.
- Zachut M, Sood P, Levin Y, Moallem U. Proteomic analysis of preovulatory follicular fluid reveals differentially abundant proteins in less fertile dairy cows. Journal of Proteomics 139, 122-129.
- Zamah A M, Hassis M E, Albertolle M E, Williams K E. Proteomic analysis of human follicular fluid from fertile women. Clinical Proteomics 12, 5.
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