Morphological and proteomic characterization of sperm in a beluga whale (Delphinapterus leucas):a case report
Status In-Process Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
41557036
DOI
10.1007/s11259-025-10991-7
PII: 10.1007/s11259-025-10991-7
Knihovny.cz E-zdroje
- Klíčová slova
- Cetacean, Monodontidae, Odontocetes, Proteomic, Semen, Seminal plasma, Sperm cells,
- Publikační typ
- časopisecké články MeSH
Department of Biology Avanqua Oceanogràfic S L Valencia 46013 Spain
Department of Biotechnology University of Alicante Alicante Spain
Research Department Fundación Oceanogràfic de la Comunitat Valenciana Valencia 46013 Spain
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Alves LQ, Ruivo R, Valente R, Fonseca MM, Machado AM, Plön S, Monteiro N, García-Parraga D, Ruiz-Díaz S, Sánchez-Calabuig MJ, Gutiérrez-Adán A, Castro LFC (2021) A drastic shift in the energetic landscape of toothed whale sperm cells. Curr Biol 31:3648-3655e9. https://doi.org/10.1016/j.cub.2021.05.062 PubMed DOI
Amaral A, Castillo J, Ramalho-Santos J, Oliva R (2014) The combined human sperm proteome: cellular pathways and implications for basic and clinical science. Hum Reprod Update 20:40–62. https://doi.org/10.1093/humupd/dmt046 PubMed DOI
Anderson PA, Poe RB, Thompson LA, Weber N, Romano TA (2017) Behavioral responses of beluga whales (Delphinapterus leucas) to environmental variation in an Arctic estuary. Behav Processes 145:48–59. https://doi.org/10.1016/j.beproc.2017.09.007 PubMed DOI
Ashwitha A, Ramesha KP, Ramesh P, Kootimole CN, Devadasan MJ, Ammankallu S, Jeyakumar S, Kumaresan A, Veerappa VG, Das DN, Prasad TSK (2023) Quantitative proteomics profiling of spermatozoa and seminal plasma reveals proteins associated with semen quality in Bos indicus bulls. J Proteomics 273:104794. https://doi.org/10.1016/j.jprot.2022.104794 PubMed DOI
Baker MA, Hetherington L, Reeves GM, Aitken RJ (2008) The mouse sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification. Proteomics 8:1720–1730. https://doi.org/10.1002/pmic.200701020 PubMed DOI
Barth AD (1989) Abaxial tail attachment of bovine spermatozoa and its effect on fertility. Can Vet J 30:656–662 PubMed PMC
Boulanger J, Faulds D, Eddy EM, Lingwood CA (1995) Members of the 70 kDa heat shock protein family specifically recognize sulfoglycolipids: role in gamete recognition and mycoplasma-related infertility. J Cell Physiol 165:7–17. https://doi.org/10.1002/jcp.1041650103 PubMed DOI
Busso D, Oñate-Alvarado MJ, Balboa E, Castro J, Lizama C, Morales G, Vargas S, Härtel S, Moreno RD, Zanlungo S (2014) Spermatozoa from mice deficient in Niemann-Pick disease type C2 (NPC2) protein have defective cholesterol content and reduced in vitro fertilising ability. Reprod Fertil Dev 26:609–621. https://doi.org/10.1071/RD12059 PubMed DOI
Bustamante-Filho IC, Pasini M, Moura AA (2022) Spermatozoa and seminal plasma proteomics: too many molecules, too few markers. The case of bovine and porcine semen. Anim Reprod Sci 247:107075. https://doi.org/10.1016/j.anireprosci.2022.107075 PubMed DOI
Calle PP, Cook RA, McClave C, Palma S (1993) Circulating gestational progesterone and estradiol concentrations, parturition, and placental descriptions of two beluga whales (Delphinapterus leucas). Proc Inter Assoc Aquatic Anim Medic 24:61
Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 38:5825–5829 PubMed DOI PMC
Castillo J, de la Iglesia A, Leiva M, Jodar M, Oliva R (2023) Proteomics of human spermatozoa. Hum Reprod 38:2312–2320. https://doi.org/10.1093/humrep/dead170 PubMed DOI
Cayli S, Jakab A, Ovari L, Delpiano E, Celik-Ozenci C, Sakkas D, Ward D, Huszar G (2003) Biochemical markers of sperm function: male fertility and sperm selection for ICSI. Reprod Biomed Online 7(4):462–468. https://doi.org/10.1016/s1472-6483(10)61891-3
Cheng G, Ke D, Rao M, Hu S, Wang Y, Zhou F, Liu H, Zhu C, Xia W (2019) Effects of cold-inducible RNA-binding protein on the proliferation and apoptosis of spermatogenic cells in vitro following heat stress. Reprod Fertil Dev 31:953–961. https://doi.org/10.1071/RD18469 PubMed DOI
Ciereszko A, Dietrich MA, Nynca J (2017) Fish semen proteomics—new opportunities in fish reproductive research. Aquaculture 472:81–92. https://doi.org/10.1016/j.aquaculture.2016.03.005 DOI
R Core Team (2024) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Cummins JM, Woodall PF (1985) On mammalian sperm dimensions. J Reprod Fertil 75:153–175 PubMed DOI
De Lazari FL, Sontag ER, Schneider A, Moura AAA, Vasconcelos FR, Nagano CS, Mattos RC, Jobim MIM, Bustamante-Filho IC (2019) Seminal plasma proteins and their relationship with sperm motility and morphology in boars. Andrologia 51:e13222. https://doi.org/10.1111/and.13222 PubMed DOI
Dietz R, Letcher RJ, Desforges JP, Eulaers I, Sonne C, Wilson S, Andersen-Ranberg E, Basu N, Barst BD, Bustnes JO et al (2019) Current state of knowledge on biological effects from contaminants on Arctic wildlife and fish. Sci Total Environ 696:133792. https://doi.org/10.1016/j.scitotenv.2019.133792 DOI
Dun MD, Smith ND, Baker MA, Lin M, Aitken RJ, Nixon B (2011) The chaperonin containing TCP1 complex (CCT/TRiC) is involved in mediating sperm–oocyte interaction. J Biol Chem 286:36875–36887. https://doi.org/10.1074/jbc.M110.188888 PubMed DOI PMC
Favilla AB, Horning M, Costa DP (2021) Advances in thermal physiology of diving marine mammals: the dual role of peripheral perfusion. Temperature 9(1):46–66. https://doi.org/10.1080/23328940.2021.1988817 DOI
Frost KJ, Russell RB, Lowry LF (1992) Killer whales, orcinus orca, in the southeastern bering sea: recent sightings and predation on other marine mammals. Mar Mamm Sci 8:110–119. https://doi.org/10.1111/j.1748-7692.1992.tb00370.x DOI
Fuentes-Albero MC, Abril Sánchez S, Ros-Santaella JL, Pintus E, Luongo C, Ruiz Díaz S, Barros García C, Sánchez Calabuig MJ (2021a) García Párraga D, García Vázquez FA Characterization of bottlenose dolphin (Tursiops truncatus) sperm based on morphometric traits. Biology 10:355. https://doi.org/10.3390/biology10050355 PubMed DOI PMC
Fuentes-Albero MC, González-Brusi L, Cots P, Luongo C, Abril-Sánchez S, Ros-Santaella JL, Pintus E, Ruiz-Díaz S, Barros-García C, Sánchez-Calabuig MJ, García-Párraga D, Avilés M, Izquierdo Rico MJ, García-Vázquez FA (2021b) Protein identification of spermatozoa and seminal plasma in bottlenose Dolphin (Tursiops truncatus). Front Cell Dev Biol 9:673961. https://doi.org/10.3389/fcell.2021.673961 PubMed DOI PMC
Fujihara Y, Satouh Y, Inoue N, Isotani A, Ikawa M, Okabe M (2012) SPACA1-deficient male mice are infertile with abnormally shaped sperm heads reminiscent of globozoospermia. Development 139:3583–3589. https://doi.org/10.1242/dev.081778 PubMed DOI
Fukuda A, Osawa T, Oda H, Tanaka T, Toyokuni S, Uchida K (1996) Oxidative stress response in iron-induced acute nephrotoxicity: enhanced expression of heat shock protein 90. Biochem Biophys Res Commun 219:76–81. https://doi.org/10.1016/0006-291X(96)91542-7 PubMed DOI
Hamil KG, Liu Q, Sivashanmugam P, Anbalagan M, Yenugu S, Soundararajan R, Grossman G, Rao AJ, Birse CE, Ruben SM, Richardson RT, Zhang YL, O’Rand MG, Petrusz P, French FS, Hall SH (2003) LCN6, a novel human epididymal Lipocalin. Reprod Biol Endocrinol 1:112. https://doi.org/10.1186/1477-7827-1-112 PubMed DOI PMC
Hopkins BR, Sepil I, Thézénas ML, Craig JF, Miller T, Charles PD, Fischer R, Kessler BM, Bretman A, Pizzari T, Wigby S (2019) Divergent allocation of sperm and the seminal proteome along a competition gradient in drosophila melanogaster. Proc Natl Acad Sci USA 116:17925–17933. https://doi.org/10.1073/pnas.1906149116 PubMed DOI PMC
Huerta-Retamal N, Sáez-Espinosa P, Robles-Gómez L, Avilés M, Romero A, Aizpurua J, Gómez-Torres MJ (2021) Human sperm chaperone HSPA2 distribution during in vitro capacitation. J Reprod Immunol 143:103246. https://doi.org/10.1016/j.jri.2020.103246
Inaba K (2003) Molecular architecture of the sperm flagella: molecules for motility and signaling. Zoolog Sci 20(9):1043–1056. https://doi.org/10.2108/zsj.20.1043 PubMed DOI
Intasqui P, Camargo M, Antoniassi MP, Cedenho AP, Carvalho VM, Cardozo KHM, Zylbersztejn DS, Bertolla RP (2016) Association between the seminal plasma proteome and sperm functional traits. Fertil Steril 105(3):617–628. https://doi.org/10.1016/j.fertnstert.2015.11.005
Karlsson M, Zhang C, Méar L, Zhong W, Digre A, Katona B, Sjöstedt E, Butler L, Odeberg J, Dusart P, Edfors F, Oksvold P, von Feilitzen K, Zwahlen M, Arif M, Altay O, Li X, Ozcan M, Mardinoglu A, Fagerberg L, Mulder J, Luo Y, Ponten F, Uhlén M, Lindskog C (2021) A single–cell type transcriptomics map of human tissues. Sci Adv 7(31):eabh2169. https://doi.org/10.1126/sciadv.abh2169 PubMed DOI PMC
Kubota H, Hynes G, Willison K (1995) The chaperonin containing t-complex polypeptide 1 (TCP-1). Multisubunit machinery assisting in protein folding and assembly in the eukaryotic cytosol. Eur J Biochem 230:3–16. https://doi.org/10.1111/j.1432-1033.1995.tb20527.x PubMed DOI
Leung MR, Zeng J, Wang X, Roelofs MC, Huang W, Zenezini Chiozzi R, Hevler JF, Heck AJR, Dutcher SK, Brown A, Zhang R, Zeev-Ben-Mordehai T (2023) Structural specializations of the sperm tail. Cell 186(13):2880-2896e17. https://doi.org/10.1016/j.cell.2023.05.026 PubMed DOI PMC
Liang Z, Dai C, He F, Wang Y, Huang Y, Li H, Wu Y, Hu Y, Xu K (2024) AKAP3-mediated typeI PKA signaling is required for mouse sperm hyperactivation and fertility†. Biol Reprod 110(4):684–697. https://doi.org/10.1093/biolre/ioad180
Liao TT, Xiang Z, Zhu WB, Fan LQ (2009) Proteome analysis of round-headed and normal spermatozoa by 2-D fluorescence difference gel electrophoresis and mass spectrometry. Asian J Androl 11(6):683–693. https://doi.org/10.1038/aja.2009.59
Lowry L, Reeves R, Laidre K (2017) Delphinapterus leucas. The IUCN Red List of Threatened Species 2017. https://doi.org/10.2305/IUCN.UK.2017-3.RLTS.T6335A50352346.en
Luongo C, González-Brusi L, Cots-Rodríguez P, Izquierdo-Rico MJ, Avilés M, García-Vázquez FA (2020) Sperm proteome after interaction with reproductive fluids in porcine: from the ejaculation to the fertilization site. Int J Mol Sci 21:6060. https://doi.org/10.3390/ijms21176060 PubMed DOI PMC
Mandal DK, Kumar M, Tyagi S (2010) Effect of age on spermiogram of Holstein Friesian × Sahiwal crossbred bulls. Animal 4:595–603. https://doi.org/10.1017/S1751731109991273 PubMed DOI
Martínez-Heredia J, Estanyol JM, Ballescà JL, Oliva R (2006) Proteomic identification of human sperm proteins. Proteomics 6:4356–4369. https://doi.org/10.1002/pmic.200600094 PubMed DOI
Meisner AD, Klaus AV, O’Leary MA (2005) Sperm head morphology in 36 species of artiodactylans, perissodactylans, and cetaceans (Mammalia). J Morphol 263:179–202. https://doi.org/10.1002/jmor.10326 DOI
Melero M, Rodríguez-Prieto V, Rubio-García A, García-Párraga D, Sánchez-Vizcaíno JM (2015) Thermal reference points as an index for monitoring body temperature in marine mammals. BMC Res Notes 8:411. https://doi.org/10.1186/s13104-015-1383-6 PubMed DOI PMC
Menezes EB, de Oliveira RV, van Tilburg MF, Barbosa EA, Nascimento NV, Velho ALMCS, Moreno FB, Moreira RA, Monteiro-Moreira ACO, Carvalho GMC, Ramos AF, Memili E, Moura AA (2017) Proteomic analysis of seminal plasma from locally-adapted Curraleiro Pé-duro bulls (Bos taurus): identifying biomarkers involved in sperm physiology in endangered animals for conservation of biodiversity. Anim Reprod Sci 183:86–101. https://doi.org/10.1016/j.anireprosci.2017.05.014 PubMed DOI
Miller DL, Styer EL, Decker SJ, Robeck TR (2002) Ultrastructure of the spermatozoa from three odontocetes: a killer whale (Orcinus orca), a Pacific white-sided dolphin (Lagenorhynchus obliquidens), and a beluga (Delphinapterus leucas). Anat Histol Embryol 31:158–168. https://doi.org/10.1046/j.1439-0264.2002.00385.x PubMed DOI
O’Brien JK, Robeck TR (2010) Preservation of beluga (Delphinapterus leucas) spermatozoa using a trehalose-based cryodiluent and directional freezing technology. Reprod Fertil Dev 22:653–663. https://doi.org/10.1071/RD09176 PubMed DOI
O’Brien JK, Steinman KJ, Schmitt TL, Robeck TR (2008) Semen collection, characterisation and artificial insemination in the Beluga (Delphinapterus leucas) using liquid-stored spermatozoa. Reprod Fertil Dev 20:770–783. https://doi.org/10.1071/RD08031 PubMed DOI
Oberska P, Grabowska M, Marynowska M, Murawski M, Gączarzewicz D, Syczewski A, Michałek K (2024) Cellular distribution of aquaporin 3, 7 and 9 in the male reproductive system: a lesson from bovine study (Bos taurus). Int J Mol Sci 25:1567. https://doi.org/10.3390/ijms25031567 PubMed DOI PMC
Pant HC, Mittal AK, Patel SH, Shukla HR, Kasiraj R, Prabhakar JH, Barot LR (2002) Abaxial sperm tails and fertility in Buffalo bull. Indian J Anim Sci 72:314–315
Peddinti D, Nanduri B, Kaya A, Feugang JM, Burgess SC, Memili E (2008) Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol 2:19. https://doi.org/10.1186/1752-0509-2-19 PubMed DOI PMC
Pintus E, Ros-Santaella JL (2018) Assessment of reproductive traits in male Gemsbok (Oryx gazella): (Bovidae, Hippotraginae). Spixiana 41:205–209
Powers MV, Clarke PA, Workman P (2008) Dual targeting of HSC70 and HSP72 inhibits HSP90AA1 function and induces tumor-specific apoptosis. Cancer Cell 14:250–262. https://doi.org/10.1016/j.ccr.2008.09.004 PubMed DOI
Purandhar K, Jena PK, Prajapati B, Rajput P, Seshadri S (2014) Understanding the role of heat shock protein isoforms in male fertility, aging and apoptosis. World J Mens Health 32(3):123–132. https://doi.org/10.5534/wjmh.2014.32.3.123
Raverty S, Nielsen O, Nielsen K, Burek K, Reynolds J (2007) Post mortem findings of hunter harvested beluga whales in the Western Arctic 2004 and 2005: possible sentinels of ecosystem change and subsistence community health. In: Program of the 1st International Workshop on Beluga Whale Research, Husbandry and Management in Wild and Captive Environments, Abstract 5, Valencia, Spain
Rice DW (1998) Marine mammals of the world: systematics and distribution. Special Publication No. 4, Society for Marine Mammalogy, Lawrence, KS
Robeck TR, Steinman KJ, Montano GA, Katsumata E, Osborn S, Dalton L, Dunn JL, Schmitt T, Reidarson T, O’Brien JK (2010) Deep intra-uterine artificial inseminations using cryopreserved spermatozoa in Beluga (Delphinapterus leucas). Theriogenology 74:989–1001. https://doi.org/10.1016/j.theriogenology.2010.04.028 PubMed DOI
Ros-Santaella JL, Domínguez-Rebolledo ÁE, Garde JJ (2014) Sperm flagellum volume determines freezability in red deer spermatozoa. PLoS One 9:e112382. https://doi.org/10.1371/journal.pone.0112382 PubMed DOI PMC
Rotman T, Etkovitz N, Spiegel A, Rubinstein S, Breitbart H (2010) Protein kinase A and protein kinase Cα/PPP1CC2 play opposing roles in the regulation of phosphatidylinositol 3-kinase activation in bovine sperm. Reproduction 140(1):43–56. https://doi.org/10.1530/REP-09-0314 PubMed DOI
Schimming BC, Baumann C, Pinheiro P, Domeniconi RF (2017) Aquaporin 9 is expressed in the epididymis of immature and mature pigs. Reprod Domest Anim 52:617–624. https://doi.org/10.1111/rda.12957 PubMed DOI
Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC, Imamichi T, Chang W (2022) DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Res. https://doi.org/10.1093/nar/gkac194
Shevchenko A, Jensen ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O, Mortensen P, Boucherie H, Mann M (1996) Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci USA 93:14440–14445 PubMed DOI PMC
Soleilhavoup C, Tsikis G, Labas V, Harichaux G, Kohnke PL, Dacheux JL, Guérin Y, Gatti JL, de Graaf SP, Druart X (2014) Ram seminal plasma proteome and its impact on liquid preservation of spermatozoa. J Proteom 109:245–260. https://doi.org/10.1016/j.jprot.2014.07.007 DOI
Vijayaraghavan S, Liberty GA, Mohan J, Winfrey VP, Olson GE, Carr DW (1999) Isolation and molecular characterization of AKAP110, a novel sperm-specific protein kinase A–anchoring protein. Mol Endocrinol 13(5):705–717. https://doi.org/10.1210/mend.13.5.0278
Vizel R, Hillman P, Ickowicz D, Breitbart H (2015) AKAP3 degradation in sperm capacitation is regulated by its tyrosine phosphorylation. Biochim Biophys Acta 1850:1912–1920. https://doi.org/10.1016/j.bbagen.2015.06.005 PubMed DOI
Wenzel GW (2009) Canadian Inuit subsistence and ecological instability—if the climate changes, must the Inuit? Polar Res 28:89–99. https://doi.org/10.1111/j.1751-8369.2009.00098.x DOI
Wittayarat M, Pukazhenthi BS, Tipkantha W, Techakumphu M, Srisuwatanasagul S, Panyaboriban S (2021) CRISP protein expression in semen of the endangered Malayan Tapir (Tapirus indicus). Theriogenology 172:106–115. https://doi.org/10.1016/j.theriogenology.2021.06.005 PubMed DOI
Xu K, Yang L, Zhang L, Qi H (2020) Lack of AKAP3 disrupts integrity of the subcellular structure and proteome of mouse sperm and causes male sterility. Development 147:dev181057. https://doi.org/10.1242/dev.181057 PubMed DOI
Yin Q, Shen J, Wan X, Liu Q, Zhou Y, Zhang Y (2018) Impaired sperm maturation in conditional Lcn6 knockout mice. Biol Reprod 98:28–41. https://doi.org/10.1093/biolre/iox128 PubMed DOI