Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
Shopping Cart: ( empty )
You are here: Home > Journals > RD > RD24014
RESEARCH ARTICLE
Contents Vol 36(5)

The case for considering the term ‘mitochondrial vesicle’ as a misnomer in publications about assisted reproductive technologies (ART) for amphibians

Robert K. Browne https://orcid.org/0000-0002-3172-9991 A * , Govindappa Venu https://orcid.org/0000-0003-4873-7418 B and Svetlana A. Kaurova https://orcid.org/0000-0002-2298-1597 C
+ Author Affiliations
- Author Affiliations

A Sustainability America, La Isla Road, Sarteneja, Corozal District, Belize.

B Department of Zoology, Centre for Applied Genetics, Jnana Bharathi Campus, Bangalore University, Bengaluru, Karnataka 560056, India.

C Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow Region 142290, Russia.

* Correspondence to: robert.browne@gmail.com

Handling Editor: Graeme Martin

Reproduction, Fertility and Development 36, RD24014 https://doi.org/10.1071/RD24014
Submitted: 31 January 2024  Accepted: 5 February 2024  Published online: 28 February 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

The term ‘mitochondrial vesicle’ was first used in 2003 in a description of anuran sperm and persists to this day throughout the literature on assisted reproductive technologies (ART) for amphibians. In the present paper, we argue that the term is inappropriate because the widely accepted definition of a ‘vesicle’ refers to an integral structure with an enclosing lipid bilayer/membrane. Moreover, there are no electron micrographs that show a vesicular structure encapsulating mitochondria on amphibian sperm heads in the literature. In fact, in 1993, the mitochondria in the anuran sperm head had been described as positioned in ‘mitochondrial collars’ or ‘mitochondrial sheaths’ surrounded by the plasma membrane of the sperm head. On the other hand, mitochondrial-derived vesicles are defined as vesicles shed from mitochondria surfaces, potentially creating confusion. Therefore, our view is that the term ‘mitochondrial vesicle’ should be avoided in describing the positioning of mitochondria on sperm.

Keywords: amphibian, anuran sperm, ART, assisted reproductive technology, mitochondrial collar, mitochondrial sheath, mitochondrial vesicle, motility, swimming.

References

Aguiar O, Giaretta AA, Recco-Pimentel SM (2006) The sperm of Hylodinae species (Anura, Leptodactylidae): ultrastructural characteristics and their relevance to interspecific taxonomic relationships. Journal of Biosciences 31, 379-388.
| Crossref | Google Scholar |

Arregui L, Kouba AJ, Germano JM, Barrios L, Moore M, Kouba CK (2022) Fertilization potential of cold-stored Fowler’s toad (Anaxyrus fowleri) spermatozoa: temporal changes in sperm motility based on temperature and osmolality. Reproduction, Fertility and Development 34(4–5), 461-469.
| Crossref | Google Scholar |

Braz SV, Fernandes AP, Bao SN (2004) An ultrastructural study of sperm of the genus Bufo (Amphibia, Anura, Bufonidae). Journal of Submicroscopic Cytology and Pathology 36(3–4), 257-262.
| Google Scholar | PubMed |

Browne RK, Kaurova SA, Uteshev VK, Shishova NV, McGinnity D, Figiel CR, Mansour N, Agnew D, Wu M, Gakhova EN, Dzyuba B, Cosson J (2015) Sperm motility of externally fertilizing fish and amphibians. Theriogenology 83(1), 1-13.e8.
| Crossref | Google Scholar | PubMed |

Burger IJ, Lampert SS, Kouba CK, Morin DJ, Kouba AJ (2022) Development of an amphibian sperm biobanking protocol for genetic management and population sustainability. Conservation Physiology 10(1), coac032.
| Crossref | Google Scholar |

Burger IJ, Chen L-D, Lampert SS, Kouba CK, Barber D, Smith D, Cobos C, Kouba AJ (2023) Applying sperm collection and cryopreservation protocols developed in a model amphibian to three threatened anuran species targeted for biobanking management. Biological Conservation 277(2), 109850.
| Crossref | Google Scholar |

Chen DM, Moore MG, Willis EL, Kouba AJ, Kouba CK (2022) The impact of time and environmental factors on the mitochondrial vesicle and subsequent motility of amphibian sperm. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 268, 111191.
| Crossref | Google Scholar |

Cruz JC, Ferraro DP, Farías A, Santos JS, Recco-Pimentel SM, Faivovich J, Hermida GN (2016) A comparative ultrastructural analysis of spermatozoa in Pleurodema (Anura, Leptodactylidae, Leiuperinae). Journal of Morphology 277, 957-977.
| Crossref | Google Scholar | PubMed |

Della Togna G (2015) Structural and functional characterization of the Panamanian golden frog (Atelopus zeteki) spermatozoa – impact of medium osmolality and cryopreservation on motility and cell viability. PhD dissertation, The Faculty of the Graduate School of the University of Maryland, College Park, USA.

Della Togna G, Gratwicke B, Evans M, Augustine L, Chia H, Bronikowski E, Murphy JB, Comizzoli P (2018) Influence of extracellular environment on the motility and structural properties of spermatozoa collected from hormonally stimulated Panamanian Golden Frog (Atelopus zeteki). Theriogenology 108, 153-160.
| Crossref | Google Scholar | PubMed |

Della Togna G, Howell LG, Clulow J, Langhorne CJ, Marcec-Greaves R, Calatayud NE (2020) Evaluating amphibian biobanking and reproduction for captive breeding programs according to the Amphibian Conservation Action Plan objectives. Theriogenology 150, 412-431.
| Crossref | Google Scholar | PubMed |

Garrido O, Pugin E, Jorquera B (1989) Sperm morphology of Batrachyla (Anura:Leptodactylidae). Amphibia-Reptilia 10, 141-149.
| Crossref | Google Scholar |

Hazan (Ben-Menachem) R, Lintzer D, Ziv T, Das K, Rosenhek-Goldian I, Porat Z, Ben Ami Pilo H, Karniely S, Saada A, Regev-Rudzki N, Pines O (2023) Mitochondrial-derived vesicles retain membrane potential and contain a functional ATP synthase. EMBO Reports 24(5), e56114.
| Crossref | Google Scholar |

Julien AR (2021) The nose glows: investigating amphibian neuroendocrine pathways with quantum dots. Theses and dissertations, Mississippi State University, Starkville, Mississippi, USA, MS 39762. Available at https://scholarsjunction.msstate.edu/td/5174

Kouba AJ, Vance CK (2009) Applied reproductive technologies and genetic resource banking for amphibian conservation. Reproduction, Fertility and Development 21(6), 719-737.
| Crossref | Google Scholar | PubMed |

Kouba AJ, Vance CK, Frommeyer MA, Roth TL (2003) Structural and functional aspects of Bufo americanus spermatozoa: effects of inactivation and reactivation. Journal of Experimental Zoology Part A: Comparative Experimental Biology 295A(2), 172-182.
| Crossref | Google Scholar | PubMed |

Kuramoto M (1998) Spermatozoa of several frog species from Japan and adjacent regions. Japanese Journal of Herpetology 17(3), 107-116.
| Crossref | Google Scholar |

Lee MSY, Jamieson BGM (1993) The ultrastructure of the spermatozoa of bufonid and hylid frogs (Anura, Amphibia): implications for phylogeny and fertilization biology. Zoologica Scripta 22(3), 309-323.
| Crossref | Google Scholar |

Lipke C, Meinecke-Tillmann S, Meyer W, Meinecke B (2009) Preparation and ultrastructure of spermatozoa from Green Poison Frogs, Dendrobates auratus, following hormonal induced spermiation (Amphibia, Anura, Dendrobatidae). Animal Reproduction Science 113(1–4), 177-186.
| Crossref | Google Scholar | PubMed |

Morshed A, Karawdeniya BI, Bandara YMNDY, Kim MJ, Dutta P (2020) Mechanical characterization of vesicles and cells: a review. Electrophoresis 41(7–8), 449-470.
| Crossref | Google Scholar |

Naranjo RE, Naydenova E, Proaño-Bolaños C, Vizuete K, Debut A, Arias MT, Coloma LA (2022) Development of assisted reproductive technologies for the conservation of Atelopus sp. (spumarius complex). Cryobiology 105, 20-31.
| Crossref | Google Scholar | PubMed |

Obringer AR, O’Brien JK, Saunders RL, Yamamoto K, Kikuyama S, Roth TL (2000) Characterization of the spermiation response, luteinizing hormone release and sperm quality in the American toad (Bufo americanus) and the endangered Wyoming toad (Bufo baxteri). Reproduction, Fertility and Development 12(2), 51-58.
| Crossref | Google Scholar | PubMed |

Poo S, Hinkson KM (2019) Applying cryopreservation to anuran conservation biology. Conservation Science and Practice 1(9), e91.
| Crossref | Google Scholar |

Popov L-D (2022) Mitochondrial-derived vesicles: recent insights. Journal of Cellular and Molecular Medicine 26(12), 3323-3328.
| Crossref | Google Scholar | PubMed |

Pugin-Rios E (1980) Etude Comparative sur la Structure du Spermatozoide des Amphibiens Anoures. Comportement des Gametes lors de la Ficondation. p. 114. PhD These, L’Universite de Rennes, France.

Roth TL, Obringer AR (2003) Reproductive research and the worldwide amphibian extinction crisis. In ‘Reproductive sciences and integrated conservation’. (Eds WV Holt, AR Pickard, JC Rodger, DE Wildt) pp. 359–374. (Cambridge University Press)

Scheltinga DM, Jamieson BGM (2003) Spermatogenesis and the mature spermatozoon: form, function and phylogenetic implications. In ‘Reproductive biology and phylogeny of Anura’. (Ed. BGM Jamieson) pp. 119–252. (Science Publishers, Inc.)

Shishova NR, Uteshev VK, Kaurova SA, Browne RK, Gakhova EN (2011) Cryopreservation of hormonally induced sperm for the conservation of threatened amphibians with Rana temporaria as a model research species. Theriogenology 75(2), 220-232.
| Crossref | Google Scholar | PubMed |

Valchi P, Ponssa ML, Farías A, Volonteri MC, Hermida GN (2023) Comparative spermatozoa ultrastructure of neotropical grass frogs (genus Leptodactylus) with comments on anuran reproductive modes and phylogeny. Zoologischer Anzeiger 302, 166-185.
| Crossref | Google Scholar |

Vance CK, Kouba AJ, Roth TL (2001) Inactivation and reactivation of spermatozoa collected in the urine from the common American toad (Bufo americanus). Theriogenology 55, 402.
| Google Scholar |

Waggener WL, Carroll EJ, Jr (1998) Spermatozoon structure and motility in the anuran Lepidobatrachus laevis. Development, Growth & Differentiation 40(1), 27-34.
| Crossref | Google Scholar |

Xing L-M, Xiao W, Li L-L, Zhang L-P, Sai Q-Y, Yu Z-X, Wu X-D, Lian Z-Q (2021) Study of sperm cryopreservation in Silurus lanzhouensis and detection of cell damages after cryopreservation. Acta Hydrobiologica Sinica 45(3), 547-556.
| Crossref | Google Scholar |

Yoshida S (2016) From cyst to tubule: innovations in vertebrate spermatogenesis. WIREs Developmental Biology 5(1), 119-131.
| Crossref | Google Scholar | PubMed |