Oxana L. Kolomiets: 42 Years at the Forefront of Meiotic Chromosome Study

To our deepest regret, on April 22, our beloved colleague and mentor Oxana Leonidovna Kolomiets (1946–2024) passed away at the age of 78. Professor O.L. Kolomiets (Fig. 1), PhD, DSc Biology, who was a leading Soviet and Russian cell biologist, cytogeneticist, and researcher of meiosis, traveled an incredible scientific journey over more than 50 years.

Oxana became interested in biology as early as grade school. This was inevitable, given that she was born into a family of doctors. Oxana took her first real steps in science during her university years. She studied chromatin in interphase nuclei, namely, specific features of structural organization of the Barr body in cat liver nuclei under the supervision of Prof. Yuri S. Chentsov at the M.V. Lomonosov Moscow State University (MSU). Her first publications were about these findings [1].

In the 1970s, Oxana investigated the progression of virus-induced tumors. Her major breakthroughs were made in electron-microscopic studies on patterns of cytodifferentiation during the growth of malignant hemangiopericytomas induced by adenoviruses, of leiomyosarcomas, and rhabdomyosarcomas induced by Rous sarcoma virus, in various experimental models [2‒5]. These discoveries and findings constituted her PhD thesis under the supervision of Dr. Inessa S. Levenbook in the Laboratory of Pathomorphology at the L.A. Tarasevich State Research Institute for the Standardization and Control of Medical Biological Preparations that was defended in 1977 at MSU [6].

In 1982, Oxana was invited by Prof. Yuri F. Bogdanov to the Laboratory of Cytogenetics at the Institute of General Genetics (USSR Academy of Sciences) and for the next 42 years she researched the mysteries of meiosis [7]. Oxana was the first in the former Soviet Union to incorporate into experimental meiosis research the electron-microscopic and immunocytochemical analysis of total spread synaptonemal complexes (SCs) after a hypotonic shock treatment. This approach allowed germ cells to be karyotyped using SCs [8].

Oxana, together with her colleagues, was one of the first in Russia to use an immunocytochemical technique for meiotic cells [9]. In the early and mid-90s, she published a series of research articles on the dynamics of spontaneous autoantibody formation against the SCs and about the localization of RecA-like proteins in mouse spermatocytes [9‒11]. From the late 2000s, immunocytochemistry and immuno-FISH became the main methods used by Oxana and her collaborators.

Oxana diligently studied various species of animals and plants (Fig. 2a–d), with a special emphasis on heterozygotes carrying reciprocal, non-reciprocal, and Robertsonian translocations to explore the mechanisms behind pachytene arrest. She and her colleagues discovered several common patterns of chromosome synapsis that can reduce fertility or cause complete sterility: chromosome co-orientation disorders, stretching of chromosomes between their attachment points to the nuclear membrane, delayed formation of axial elements and SCs in translocation zones, correction of synapsis of heteromorphic chromosomes at the late pachytene stage, and formation of complex SC chains due to heterochromatin segments and/or monobrachial homologies (Fig. 2a) [12‒15]. Oxana paid particular attention to the phenomenon of desynapsis, which can serve as either a trigger or a barrier to further events. She discovered for the first time that in the Korean field mouse, B chromosomes may be involved in the formation of complex multivalents (i.e., hexavalents) at prophase I and that this phenomenon may be due to partial homology of the B and standard chromosomes (Fig. 2c, 3) [16].

The most interesting results during this period were obtained in her study on nonstandard sex chromosomes of mammals: she discovered functional heteromorphism of two male X chromosomes in the prophase I in three sibling species of mole voles Ellobius (and showed that this heteromorphism is probably due to epigenetic mechanisms), partial meiotic silencing of a sex trivalent in male common shrews, and other phenomena [19‒21].

Throughout Oxana’s scientific career at the Laboratory of Cytogenetics she and those working with her studied the ultrastructural organization of SCs and patterns of chromosome synapsis. They gave special attention to distinct features of attachment of chromatin loops to SCs in mice and humans [22, 23], chromosome synapsis in meiocytes of the domestic chicken Gallus gallus (Fig. 2b) [17], microsporocytes of common wheat Triticum aestivum [24], disassembly of SCs at the diplotene stage in rye microsporocytes [25], organization of centromeres [15, 26, 27] and telomeres [28], specific synapsis in trivalents of heterozygous mole voles (the terms “quick” and “slow” trivalents were introduced) [12‒14], and the behavior and evolution of sex chromosomes in various vertebrate taxa [19‒21, 29, 30]. Oxana was the pioneer in utilizing the surface spreads technique (SC spreads) for analyzing microsporocytes in Hordeum vulgare (common barley) (Fig. 2e) [8] and among the earliest researchers to apply this method to spermatocytes of Bombyx mori (silkworm) [31].

For the first time in the USSR, Oxana and colleagues studied the effects of ionizing radiation on mammalian germ cells at the ultrastructural level and traced the consequences, leading to decreased fertility (Fig. 2f) [18, 32, 33]. The effects of space flight on meiotic chromosomes and reproductive function in male rats were studied following their mission aboard the Cosmos-1667 satellite [34]. A series of articles by Oxana deals with research into the damaging effects of antimicrobial antibiotics, prescription drugs, antitumor therapeutics, rocket fuel components, and other chemical agents on murine meiotic chromosomes [35‒39].

Oxana was especially interested in human meiosis (Fig. 2e) and fertility disorders. She examined meiotic chromosomes of patients with azoospermia and severe forms of oligozoospermia as well as in cases with Sertoli cell-only syndrome [40‒44]. She paid particular attention to the problem of idiopathic infertility. Undoubtedly, her articles describing the applicability of germline cell analyses to the diagnosis of meiotic infertility had an impact on medical research at reproductive-health centers [45].

Oxana’s input into research on spermatogenesis should be highlighted. Her laboratory pioneered techniques for obtaining squashed cells from seminiferous tubules of animals and humans to investigate three-dimensional in situ chromatin organization. They investigated the processes of autophagy and apoptosis in experimental models with varying levels of infertility. This research had a particular focus on the role of Sertoli cells in spermatogenesis [46, 47].

The work of Oxana and her followers on meiosis in automictic organisms generated fascinating results. For instance, in the assembly of meiotic chromosome axes, substantial disturbances were demonstrated in the apomictic white button mushroom (which is cultivated on a large industrial scale in many countries) that are associated with the suppression of meiotic recombination [48]. Other studies on meiosis in parthenogenetic rock lizards allowed premeiotic endoduplication to be visualized and the SCs in rare polyploid oocytes to be described. Her study on triploid hybrid rock lizard males uncovered specific features of competitive synapsis of chromosomes in spermatocyte nuclei and the ability of germline cells to overcome the occurrence of both meiotic divisions as well as the formation of aneuploid spermatids [49].

From 2006 to 2024 at the Vavilov Institute of General Genetics (Russian Academy of Sciences), Prof. O.L. Kolomiets headed one of the leading cytogenetic laboratories in Russia (Fig. 4). Oxana supervised seven PhD dissertations and was the author of more than 250 publications, in Russian and international scientific journals. She trained and mentored dozens of young scientists, many of whom are actively working in the field of cytogenetics and are proud to call Oxana their teacher. Being a top tier devoted experimenter, she continued to work right to the end of her life. The findings of numerous meiotic studies became the basis of Oxana’s Doctor of Science (DSc) dissertation, defended in 1998 [50], and were summarized in the monograph “Synaptonemal complex as an indicator of the dynamics of meiosis and chromosome variation” (published in 2007 in Russian and coauthored with Prof. Yuri F. Bogdanov) [51]. Thus, through her exceptional work, Oxana significantly deepened our understanding of the phenomenology of meiosis, illuminating its fundamental mechanisms and patterns, unraveling cytogenetic complexities within an evolutionary framework, and advancing its applications in both educational and medical practice.

Prof. O.L. Kolomiets was always a kind person willing to help others, an excellent biologist, and an attentive supervisor. Oxana enjoyed deep respect of the scientific community and the sincere love of her disciples and collaborators. The staff of her laboratory and of the Institute as well as many other colleagues will forever cherish the memory of Oxana, an outstanding researcher and empathetic human being.