Abstract
Sperm carries a reservoir of proteins regulating the molecular functions to attain functional competence. Semen samples collected from buffalo bulls were assessed for sperm functional attributes (n = 11) and proteome profiling (n = 6). Sperm proteins were extracted and profiled by employing LC–MS/MS. Overall, the buffalo sperm contained 1365 proteins, of which 458 were common between the groups. The unique proteins were 477 and 430 in good and poor quality semen, respectively. In the whole proteome of buffalo sperm, sexual reproduction with phosphatidylethanolamine-binding protein1 (PEBP1), fetuin-B (FETUB) and acrosin (ACR) was the most enriched (p = 8.44E−19) biological process, also with thermogenesis (p = 0.003), oocyte meiosis (p = 0.007) and vascular smooth muscle contraction (p = 0.009) apart from metabolic pathways. In good quality semen, mesenchyme migration (p = 1.24E−07) and morphogenesis (p = 0.001) were abundant biological processes. In good quality semen, the fluid shear stress (p = 0.01) and, in poor quality semen, valine, leucine and isoleucine degradation (p = 3.8E−05) pathways were enriched. In good quality semen, 7 proteins were significantly (p < 0.05) upregulated and 33 proteins were significantly (p < 0.05) downregulated. On validating the abundantly expressed sperm proteins, serine protease inhibitor Kazal-type 2-like (SPINK2; 2.17-fold) and neddylin (NEDD8; 1.13-fold) were upregulated and YBX2 was downregulated (0.41-fold) in good quality semen as compared with poor quality semen (1-fold). The present findings revealed the importance of sperm proteins in oocyte maturation, fertilization process and early embryonic development. The variations in the proteomic composition can be used as potential markers for the selection of breeding bulls.
Similar content being viewed by others
Change history
24 February 2021
A Correction to this paper has been published: https://doi.org/10.1007/s00441-021-03417-8
References
Agarwal A, Mulgund A, Hamada A, Chyatte MR (2015) A unique view on male infertility around the globe. Reprod Biol Endocrinol 13:37. https://doi.org/10.1186/s12958-015-0032-1
Agarwal A, Panner Selvam MK, Baskaran S (2020) Proteomic analyses of human sperm cells: understanding the role of proteins and molecular pathways affecting male reproductive health. Int J Mol Sci 21:1621. https://doi.org/10.3390/ijms21051621
Amaral A, Paiva C, Attardo Parrinello C, Estanyol JM, Ballesca JL, Ramalho-Santos J, Oliva R (2014) Identification of proteins involved in human sperm motility using high-throughput differential proteomics. J Proteome Res 13:5670–5684. https://doi.org/10.1021/pr500652y
Amini-Bavil-Olyaee S, Choi YJ, Lee JH, Shi M, Huang IC, Farzan M, Jung JU (2013) The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 13:452–464. https://doi.org/10.1016/j.chom.2013.03.006
Archana SS, Selvaraju S, Binsila BK, Arangasamy A, Krawetz SA (2019) Immune regulatory molecules as modifiers of semen and fertility: a review. Mol Reprod Dev 86:1485–1504. https://doi.org/10.1002/mrd.23263
Baena MM, Tizioto PC, Meirelles SLC, Regitano LCDA, de Almeida LC (2018) HSF1 and HSPA6 as functional candidate genes associated with heat tolerance in Angus cattle. Rev Bras Zootec 47. https://doi.org/10.1590/rbz4720160390
Bahadorani M, Tavalaee M, Abedpoor N, Ghaedi K, Nazem MN, Nasr-Esfahani MH (2019) Effects of branched-chain amino acid supplementation and/or aerobic exercise on mouse sperm quality and testosterone production. Andrologia 51:e13183. https://doi.org/10.1111/and.13183
Bansal SK, Gupta N, Sankhwar SN, Rajender S (2015) Differential genes expression between fertile and infertile spermatozoa revealed by transcriptome analysis. PLoS ONE 10. https://doi.org/10.1371/journal.pone.0127007
Baskaran S, Panner Selvam MK, Agarwal A (2020) Exosomes of male reproduction. Adv Clin Chem 95:149–163. https://doi.org/10.1016/bs.acc.2019.08.004
Bhakat M, Mohanty TK, Raina VS, Gupta AK, Khan HM, Mahapatra RK, Sarkar M (2011) Effect of age and season on semen quality parameters in Sahiwal bulls. Trop Anim Health Prod 43:1161–1168. https://doi.org/10.1007/s11250-011-9817-1
Bouckson-Castaing V, Moudjou M, Ferguson DJP, Mucklow S, Belkaid Y, Milon G, Crocker PR (1996) Molecular characterisation of ninein, a new coiled-coil protein of the centrosome. J cell Sci 109:179–190
Cao J, Xu H, Zhao H, Gong W, Dunaway-Mariano D (2009) The mechanisms of human hotdog-fold thioesterase 2 (h0054HEM2) substrate recognition and catalysis illuminated by a structure and function based analysis. Biochemistry 48:1293–1304. https://doi.org/10.1021/bi801879z
Card CJ, Anderson EJ, Zamberlan S, Krieger KE, Kaproth M, Sartini BL (2013) Cryopreserved bovine spermatozoal transcript profile as revealed by high-throughput ribonucleic acid sequencing. Biol Reprod 88:49–50. https://doi.org/10.1095/biolreprod.112.103788
Codognoto VM, Yamada PH, Schmith RA, de Ruediger FR, Scott C, de Faria LP, de Brochine S, Paula Freitas-Dell’Aqua C, de Souza Oba FFE (2018) Functional insights into the role of seminal plasma proteins on sperm motility of buffalo. Anim Reprod Sci 195:251–258. https://doi.org/10.1016/j.anireprosci.2018.06.002
Collodel G, Castellini C, Chung-Yung Lee J, Signorini C (2020) Relevance of fatty acids to sperm maturation and quality. Oxid Med Cell Longev. https://doi.org/10.1155/2020/7038124
Crisa A, Marchitelli C, Pariset L, Contarini G, Signorelli F, Napolitano F, Catillo G, Valentini A, Moioli B (2010) Exploring polymorphisms and effects of candidate genes on milk fat quality in dairy sheep. J Dairy Sci 93:3834–3845. https://doi.org/10.3168/jds.2009-3014
D’Amours O, Bordeleau LJ, Frenette G, Blondin P, Leclerc P, Sullivan R (2012) Binder of sperm 1 and epididymal sperm binding protein 1 are associated with different bull sperm subpopulations. Reproduction 143:759–771. https://doi.org/10.1530/REP-11-0392
D’Amours O, Calvo E, Bourassa S, Vincent P, Blondin P, Sullivan R (2019) Proteomic markers of low and high fertility bovine spermatozoa separated by Percoll gradient. Mol Reprod Dev 86:999–1012. https://doi.org/10.1002/mrd.23174
Danshina PV, Geyer CB, Dai Q, Goulding EH, Willis WD, Kitto GB, McCarrey JR, Eddy EM, O’Brien DA (2010) Phosphoglycerate kinase 2 (PGK2) is essential for sperm function and male fertility in mice. Biol Reprod 82:136–145. https://doi.org/10.1095/biolreprod.109.079699
de Mateo S, Castillo J, Estanyol JM, Ballesca JL, Oliva R (2011) Proteomic characterization of the human sperm nucleus. Proteomics 11:2714–2726. https://doi.org/10.1002/pmic.201000799
Erata GO, Toker NK, Durlanık O, Kadıoglu A, Aktan G, Toker GA (2008) The role of heat shock protein 70 (Hsp 70) in male infertility: is it a line of defense against sperm DNA fragmentation? Fertil Steril 90:322–327
Filippou PS, Karagiannis GS, Constantinidou A (2020) Midkine (MDK) growth factor: a key player in cancer progression and a promising therapeutic target. Oncogene 39:2040–2054. https://doi.org/10.1038/s41388-019-1124-8
Fujihara Y, Oji A, Kojima-Kita K, Larasati T, Ikawa M (2018) Co-expression of sperm membrane proteins CMTM2A and CMTM2B is essential for ADAM3 localization and male fertility in mice. J Cell Sci 131. https://doi.org/10.1242/jcs.221481
Fu Q, Pan L, Huang D, Wang Z, Hou Z, Zhang M (2019) Proteomic profiles of buffalo spermatozoa and seminal plasma. Theriogenology 134:74–82. https://doi.org/10.1016/j.theriogenology.2019.05.013
Giorgini F, Davies HG, Braun RE (2001) MSY2 and MSY4 Bind a conserved sequence in the 3′ untranslated region of protamine 1 mRNA in vitro and in vivo. Mol Cell Biol 21:7010–7019. https://doi.org/10.1128/mcb.21.20.7010-7019.2001
Gmachl M, Sagan S, Ketter S, Kreil G (1993) The human sperm protein PH-20 has hyaluronidase activity. FEBS Lett 336:545–548. https://doi.org/10.1016/0014-5793(93)80873-S
Goodarzi MO, Xu N, Cui J, Guo X, Chen YI, Azziz R (2008) Small glutamine-rich tetratricopeptide repeat-containing protein alpha (SGTA), a candidate gene for polycystic ovary syndrome. Hum Reprod 23:1214–1219. https://doi.org/10.1093/humrep/den065
Hao Y, Mathialagan N, Walters E, Mao J, Lai L, Becker D, Li W, Critser J, Prather RS (2006) Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol Reprod 75:726–733. https://doi.org/10.1095/biolreprod.106.052589
Hay ED (2005) The mesenchymal cell, its role in the embryo and the remarkable signaling mechanisms that create it. Dev Dyn 233:706–720. https://doi.org/10.1002/dvdy.20345
Hecht NB (1998) Molecular mechanisms of male germ cell differentiation. Bio Essays 20:555–561. https://doi.org/10.1002/(SICI)1521-1878(199807)
Hemachand T, Gopalakrishnan B, Salunke DM, Totey SM, Shaha C (2002) Sperm plasma-membrane-associated glutathione S-transferases as gamete recognition molecules. J Cell Sci 115:2053–2065. https://doi.org/10.1093/humrep/des452
Hereng TH, Elgstoen KBP, Cederkvist FH, Eide L, Jahnsen T, Skalhegg BS, Rosendal KR (2011) Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa. Hum Reprod 26:3249–3263. https://doi.org/10.1093/humrep/der317
Hou Z, Fu Q, Huang Y, Zhang P, Chen F, Li M, Xu Z, Yao S, Chen D, Zhang M (2019) Comparative proteomic identification buffalo spermatozoa during in vitro capacitation. Theriogenology 126:303–309. https://doi.org/10.1016/j.theriogenology.2018.12.025
Huang Q, Liu L, Wu Y, Wang X, Luo L, Nan B, Zhang J, Tian M, Shen H (2019) Seminal plasma metabolites mediate the associations of multiple environmental pollutants with semen quality in Chinese men. Environ Int 132:105066. https://doi.org/10.1016/j.envint.2019.105066
Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434:234–238. https://doi.org/10.1038/nature03362
Jalkanen J, Kotimaki M, Huhtaniemi I, Poutanen M (2006) Novel epididymal protease inhibitors with Kazal or WAP family domain. Biochem Biophys Res Commun 349:245–254. https://doi.org/10.1016/j.bbrc.2006.08.023
Jiang H, Rao KS, Yee VC, Kraus JP (2005) Characterization of four variant forms of human propionyl-CoA carboxylase expressed in Escherichia coli. J Biol Chem 280:27719–27727. https://doi.org/10.1074/jbc.M413281200
Jodar M, Sendler E, Krawetz SA (2016) The protein and transcript profiles of human semen. Cell Tissue Res 363:85–96. https://doi.org/10.1007/s00441-015-2237-1
Kherraf Z, Christou‐Kent M, Karaouzene T, Amiri‐Yekta A, Martinez G, Vargas AS, Lambert E, Borel C, Dorphin B, Aknin‐Seifer I, Mitchell MJ (2017) SPINK 2 deficiency causes infertility by inducing sperm defects in heterozygotes and azoospermia in homozygotes. EMBO Mol Med 9:1132–1149. https://doi.org/10.15252/emmm.201607461
Kleene KC (2016) Position-dependent interactions of Y-box protein 2 (YBX2) with mRNA enable mRNA storage in round spermatids by repressing mRNA translation and blocking translation-dependent mRNA decay. Mol Reprod Dev 83:190–207. https://doi.org/10.1002/mrd.22616
Kong N, Xu X, Zhang Y, Wang Y, Hao X, Zhao Y, Qiao J, Xia G, Zhang M (2017) Natriuretic peptide type C induces sperm attraction for fertilization in mouse. Sci Rep 7:1–12. https://doi.org/10.1038/srep39711
Kowalik D, Haller F, Adamski J, Moeller G (2009) In search for function of two human orphan SDR enzymes: hydroxysteroid dehydrogenase like 2 (HSDL2) and short-chain dehydrogenase/reductase-orphan (SDR-O). J Steroid Biochem Mol Biol 117:117–124. https://doi.org/10.1016/j.jsbmb.2009.08.001
Krzyzosiak J, Molan P, Vishwanath R (1999) Measurements of bovine sperm velocities under true anaerobic and aerobic conditions. Anim Reprod Sci 55:163–173. https://doi.org/10.1016/S0378-4320(99)00016-0
Lampiao F, du Plessis SS (2008) Insulin and leptin enhance human sperm motility, acrosome reaction and nitric oxide production. Asian J Androl 10:799–807. https://doi.org/10.1111/j.1745-7262.2008.00421
Lee B, Park I, Jin S, Choi H, Kwon JT, Kim J, Jeong J, Cho BN, Eddy EM, Cho C (2011) Impaired spermatogenesis and fertility in mice carrying a mutation in the Spink2 gene expressed predominantly in testes. J Biol Chem 286:29108–29117. https://doi.org/10.1074/jbc.M111.244905
Li X, Zhang N, Ye HY, Song PP, Chang W, Chen L, Wang Z, Zhang L, Wang NN (2019) HYOU1 promotes cell growth and metastasis via activating PI3K/AKT signaling in epithelial ovarian cancer and predicts poor prognosis. Eur Rev Med Pharmaco 23:4126–4135. https://doi.org/10.26355/eurrev_201901_17914
Liu X, Li Q, Wang W, Liu F (2019) Aberrant expression of sperm-specific glycolytic enzymes are associated with poor sperm quality. Mol Med Rep 19:2471–2478. https://doi.org/10.3892/mmr.2019.9926
Liu X, Huang W, Li C, Li P, Yuan J, Li X, Qiu XB, Ma Q, Cao C (2006) Interaction between c-Abl and Arg tyrosine kinases and proteasome subunit PSMA7 regulates proteasome degradation. Mol Cell 22:317–327. https://doi.org/10.1016/j.molcel.2006.04.007
Lorenzetti D, Bishop CE, Justice MJ (2004) Deletion of the Parkin coregulated gene causes male sterility in the quakingviable mouse mutant. Proc Natl Acad Sci 101:8402–8407. https://doi.org/10.1073/pnas.0401832101
Aslam M, Kumaresan MK, Yadav A, Mohanty S, Datta TK (2019) Comparative proteomic analysis of high- and low-fertile buffalo bull spermatozoa for identification of fertility-associated proteins. Reprod Domest Anim 54:786–794. https://doi.org/10.1111/rda.13426
Magdanz V, Boryshpolets S, Ridzewski C, Eckel B, Reinhardt K (2019) The motility-based swim-up technique separates bull sperm based on differences in metabolic rates and tail length. PLoS ONE 14. https://doi.org/10.1371/journal.pone.0223576
Martinez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballesca JL, Oliva R (2008) Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod 23:783–791. https://doi.org/10.1093/humrep/den024
Martinez G, Kherraf ZE, Zouari R, Fourati Ben Mustapha S, Saut A, Pernet-Gallay K, Bertrand A, Bidart M, Hograindleur JP, Amiri-Yekta A, Kharouf M (2018) Whole-exome sequencing identifies mutations in FSIP2 as a recurrent cause of multiple morphological abnormalities of the sperm flagella. Hum Reprod 33:1973–1984. https://doi.org/10.1093/humrep/dey264
Matsumoto M, Fujimoto H (1990) Cloning of a hsp70-related gene expressed in mouse spermatids. Biochem Biophys Res Commun 166:43–49. https://doi.org/10.1016/0006-291X(90)91909-C
Moein-Vaziri N, Phillips I, Smith S, Alminana C, Maside C, Gil MA, Roca J, Martinez EA, Holt WV, Pockley AG, Fazeli A (2014) Heat-shock protein A8 restores sperm membrane integrity by increasing plasma membrane fluidity. Reproduction 147:719–732. https://doi.org/10.1530/REP-13-0631
Moessinger C, Kuerschner L, Spandl J, Shevchenko A, Thiele C (2011) Human lysophosphatidylcholine acyltransferases 1 and 2 are located in lipid droplets where they catalyze the formation of phosphatidylcholine. J Biol Chem 286:21330–21339. https://doi.org/10.1074/jbc.M110.202424
Moos J, Peknicova J, Tesarik J (1993) Protein—protein interactions controlling acrosin release and solubilization during the boar sperm acrosome reaction. Biol Reprod 49:408–415. https://doi.org/10.1095/biolreprod49.2.408
Naaby-Hansen S, Herr JC (2010) Heat shock proteins on the human sperm surface. J Reprod Immunol 84:32–40. https://doi.org/10.1016/j.jri.2009.09.006
Nizza A, Dimeo C, Taranto S (2010) Effect of lysine and methionine on libido and semen characteristics of bucks. World Rabbit Sci 8:181–184. https://doi.org/10.4995/wrs.2000.437
Olahova M, Yoon WH, Thompson K, Jangam S, Fernandez L, Davidson JM, Kyle JE, Grove ME, Fisk DG, Kohler JN, Holmes M (2018) Biallelic mutations in ATP5F1D, which encodes a subunit of ATP synthase, cause a metabolic disorder. Am J Hum Genet 102:494–504. https://doi.org/10.1016/j.ajhg.2018.01.020
Ou CM, Tang JB, Huang MS, Sudhakar Gandhi PS, Geetha S, Li SH, Chen YH (2012) The mode of reproductive-derived Spink (serine protease inhibitor Kazal-type) action in the modulation of mammalian sperm activity. Int J Androl 35:52–62. https://doi.org/10.1111/j.1365-2605.2011.01159.x
Parker V, Robertson D, Wang T, Hornigold DC, Petrone M, Cooper AT, Posch MG, Heise T, Plum-Moerschel L, Schlichthaar H, Klaus B (2020) Efficacy, safety, and mechanistic insights of cotadutide, a dual receptor glucagon-like peptide-1 and glucagon agonist. J Clin Endocrinol Metab 105:803–820
Pasek RC, Malarkey E, Berbari NF, Sharma N, Kesterson RA, Tres LL, Kierszenbaum AL, Yoder BK (2016) Coiled-coil domain containing 42 (Ccdc42) is necessary for proper sperm development and male fertility in the mouse. Dev Biol 412:208–218. https://doi.org/10.1016/j.ydbio.2016.01.042
Pini T, Rickard JP, Leahy T, Crossett B, Druart X, de Graaf SP (2018) Cryopreservation and egg yolk medium alter the proteome of ram spermatozoa. J Proteomics 181:73–82. https://doi.org/10.1016/j.jprot.2018.04.001
Pinto TMF, Moreira RF, Matos MNC, Soares VV, Aguiar MV, Aragao PD, Alves Filho JG, Moreno FB, Monteiro-Moreira AC, Costa CR, Lima Filho JL (2019) Evaluation of the proteomic profiles of ejaculated spermatozoa from Saanen bucks (Capra hircus). Anim Reprod 16:902–913. https://doi.org/10.21451/1984-3143-AR2019-0001
Qin J, Lee HJ, Wu SP, Lin SC, Lanz RB, Creighton CJ, DeMayo FJ, Tsai SY, Tsai MJ (2014) Androgen deprivation–induced NCoA2 promotes metastatic and castration-resistant prostate cancer. J Clin Invest 124:5013–5026. https://doi.org/10.1172/JCI76412
Rezende FM, Dietsch GO, Penagaricano F (2018) Genetic dissection of bull fertility in US Jersey dairy cattle. Anim Genet 49:393–402. https://doi.org/10.1111/age.12710
Roca J, Perez-Patino C, Barranco I, Padilla LC, Martinez EA, Rodriguez-Martinez H, Parrilla I (2020) Proteomics in fresh and preserved pig semen: recent achievements and future challenges. Theriogenology 150:41–47. https://doi.org/10.1016/j.theriogenology.2020.01.066
Rotman T, Etkovitz N, Spiegel A, Rubinstein S, Breitbart H (2010) Protein kinase A and protein kinase C (a)/PPP1CC2 play opposing roles in the regulation of phosphatidylinositol 3-kinase activation in bovine sperm. Reproduction 140:43–56. https://doi.org/10.1530/REP-09-0314
Ruiz-Pesini E, Diez-Sanchez C, Lopez-Perez MJ, Enriquez JA (2007) The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr Top Dev Biol 77:3–19. https://doi.org/10.1016/S0070-2153(06)77001-6
Satouh Y, Inoue N, Ikawa M, Okabe M (2012) Visualization of the moment of mouse sperm-egg fusion and dynamic localization of IZUMO1. J Cell Sci 125:4985–4990. https://doi.org/10.1242/jcs.100867
Selvaraju S, Parthipan S, Somashekar L, Kolte AP, Binsila BK, Arangasamy A, Ravindra JP, (2017) Occurrence and functional significance of the transcriptome in bovine (Bos taurus) spermatozoa. Scientific Reports 7 (1)
Selvaraju S, Krishnan BB, Archana SS, Ravindra JP (2016a) IGF1 stabilizes sperm membrane proteins to reduce cryoinjury and maintain post-thaw sperm motility in buffalo (Bubalus bubalis) spermatozoa. Cryobiology 73:55–62. https://doi.org/10.1016/j.cryobiol.2016.05.012
Selvaraju S, Ravindra JP, Ghosh J, Gupta PS, Suresh KP (2008) Evaluation of sperm functional attributes in relation to in vitro sperm-zona pellucida binding ability and cleavage rate in assessing frozen thawed buffalo (Bubalus bubalis) semen quality. Anim Reprod Sci 106:311–321. https://doi.org/10.1016/j.anireprosci.2007.05.005
Selvaraju S, Somashekar L, Krishnan BB, Parthipan S, Pushparani G, Arangasamy A, Rajendran D, Ravindra JP (2016b) Relationship between seminal plasma tuberoinfundibular peptide of 39 residues and sperm functional attributes in buffalo (Bubalus bubalis). Reprod Fertil Dev 28:1622. https://doi.org/10.1071/RD15008
Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2007) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856–2860. https://doi.org/10.1038/nprot.2006.468
Singh K, Jaiswal D (2013) One-carbon metabolism, spermatogenesis, and male infertility. Reprod Sci 20:622–630. https://doi.org/10.1177/1933719112459232
Somashekar L, Selvaraju S, Parthipan S, Patil SK, Binsila BK, Venkataswamy MM, Karthik Bhat S, Ravindra JP (2017) Comparative sperm protein profiling in bulls differing in fertility and identification of phosphatidylethanolamine-binding protein 4, a potential fertility marker. Andrology 5:1032–1051. https://doi.org/10.1111/andr.12404
Stillwell EE, Zhou J, Joshi HC (2004) Human ninein is a centrosomal autoantigen recognized by CREST patient sera and plays a regulatory role in microtubule nucleation. Cell Cycle 3:921–928. https://doi.org/10.4161/cc.3.7.947
Storey BT (2008) Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 52:427–437. https://doi.org/10.1387/ijdb.072522bs
Sun Y, Zhang W, Zhao X, Yuan RP, Jiang H, Pu XP (2014) PARK7 protein translocating into spermatozoa mitochondria in Chinese asthenozoospermia. Reproduction 143:249–257. https://doi.org/10.1530/REP-14-0222
Tateishi K, Omata M, Tanaka K, Chiba T (2001) The NEDD8 system is essential for cell cycle progression and morphogenetic pathway in mice. J Cell Biol 155:571–579. https://doi.org/10.1083/jcb.200104035
Thelie A, Rehault-Godbert S, Poirier J, Govoroun M, Fouchécourt S, Blesbois E (2019) The seminal acrosin-inhibitor ClTI1/SPINK2 is a fertility-associated marker in the chicken. Mol Reprod Dev 86:762–775. https://doi.org/10.1002/mrd.23153
Toshimori K (1998) Maturation of mammalian spermatozoa: modifications of the acrosome and plasma membrane leading to fertilization. Cell Tissue Res 293:177–187
van Koningsbruggen S, Straasheijm KR, Sterrenburg E, de Graaf N, Dauwerse HG, Frants RR, van der Maarel SM (2007) FRG1P-mediated aggregation of proteins involved in pre-mRNA processing. Chromosoma 116:53–64. https://doi.org/10.1007/s00412-006-0083-3
Verma A, Rajput S, Kumar S, De S, Chakravarty AK, Kumar R, Datta TK (2015) Differential histone modification status of spermatozoa in relation to fertility of buffalo bulls. J Cell Biochem 116:743–753. https://doi.org/10.1002/jcb.25029
Visconti PE, Kopf GS (1998) Regulation of protein phosphorylation during sperm capacitation1. Biol Reprod 59:1–6. https://doi.org/10.1095/biolreprod59.1.1
Wakazono A, Fukao T, Yamaguchi S, Hori T, Orii T, Lambert M, Mitchell GA, Lee GW, Hashimoto T (1995) Molecular, biochemical, and clinical characterization of mitochondrial acetoacetyl-coenzyme A thiolase deficiency in two further patients. Hum Mutat 5:34–42. https://doi.org/10.1002/humu.1380050105
Wanggren K, Stavreus-Evers A, Olsson C, Andersson E, Gemzell-Danielsson K (2008) Regulation of muscular contractions in the human fallopian tube through prostaglandins and progestagens. Human Reprod 23(2359):2368. https://doi.org/10.1093/humrep/den260
Weber A, Argenti LE, de Souza APB, Santi L, Beys-da-Silva WO, Yates JR, Bustamante-Filho IC (2020) Ready for the journey: a comparative proteome profiling of porcine cauda epididymal fluid and spermatozoa. Cell Tissue Res 379:389–405. https://doi.org/10.1007/s00441-019-03080-0
Westfalewicz B, Dietrich MA, Mostek A, Partyka A, Bielas W, Nizanski W, Ciereszko A (2017) Identification and functional analysis of bull (Bos taurus) cauda epididymal fluid proteome. J Dairy Sci 100:6707–6719. https://doi.org/10.3168/jds.2016-12526
Yu G, Liu X, Zhang D, Wang J, Ouyang G, Chen Z, Xiao W (2019) Zebrafish Nedd8 facilitates ovarian development and the maintenance of female secondary sexual characteristics via suppression of androgen receptor activity. SSRN Electron J. https://doi.org/10.2139/ssrn.3323376
Zhu W, Zhang Y, Ren C, huan C, Cheng X, Chen JH, Ge ZY, Sun ZP, Zhuo X, Sun FF, Jia XJ, Zhang Z (2020) Identification of proteomic markers for ram spermatozoa motility using a tandem mass tag (TMT) approach. J Proteomics 210:103438. https://doi.org/10.1016/j.jprot.2019.103438
Zimmerman S, Sutovsky P (2009) The sperm proteasome during sperm capacitation and fertilization. J Reprod Immunol 83:19–25. https://doi.org/10.1016/j.jri.2009.07.006
Acknowledgments
The study was supported by ICAR-All India Coordinated Research Project on “Nutritional and physiological interventions for enhancing reproductive performance in animals.” The authors sincerely acknowledge the support of the Director, ICAR-NIANP, Bangalore, and Coordinator AICRP for conducting research at ICAR-NIANP. The authors sincerely thank Dr. J.P Ravindra, Former Head, Animal Physiology Division, ICAR-NIANP for the technical inputs and critical reviewing of the manuscript. Dr. S. Selvaraju is supported by ICAR-National Fellow Project, ICAR, Ministry of Agriculture, Government of India.
Author information
Authors and Affiliations
Contributions
BBK, SS and NSKG: designed the experiment; ASS, RL and SD: performed experiments; RA: data interpretation; BBK, SS, ASS and NSKG: wrote the paper; RB: critically discussed the data; BBK, SS, NSKG and DTP: critically discussed the data, carried out data interpretation and prepared manuscript. All authors reviewed the manuscript.
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Binsila, B.K., Archana, S.S., Ramya, L. et al. Elucidating the processes and pathways enriched in buffalo sperm proteome in regulating semen quality. Cell Tissue Res 383, 881–903 (2021). https://doi.org/10.1007/s00441-020-03303-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-020-03303-9