CRYOBANKING OF SOMATIC CELLS IN CONSERVATION OF ANIMAL GENETIC RESOURCES: PROSPECTS AND SUCCESSES (review)
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SEL’SKOKHOZYAISTVENNAYA BIOLOGIYA [AGRICULTURAL BIQLQGY1, 2014, № 6, pp. 3−14
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UDC 636. 01+502. 74):57. 086. 13 doi: 10. 15 389/agrobiology. 2014.6. 3rus
doi: 10. 15 389/agrobiology. 2014.6. 3eng
CRYOBANKING OF SOMATIC CELLS IN CONSERVATION OF ANIMAL GENETIC RESOURCES: PROSPECTS AND SUCCESSES
G.N. SINGINA, N.A. VOLKOVA, V.A. BAGIROV, N.A. ZINOVIEVA
All-Russian Research Institute of Animal Husbandry, Russian Academy of Agricultural Sciences, pos. Dubrovitsy, Podolsk Region, Moscow Province, 142 132 Russia, e-mail g_singina@mail. ru, natavolkova@inbox. ru, vugarbagi-rov@mail. ru, n_zinovieva@mail. ru
Supported by the Ministry of Education and Science of the Russian Federation Received August 18, 2014
Extinction of many species is irreversible and is a part of the natural evolution, but human activities have influenced this process, making it much faster comparing to speciation. According to FAO, approximately 20% of the breeds of cattle, goats, pigs, horses and poultry in the world are currently at risk of disappearance, many have died in the past few years, as a result their genetic characteristics lost forever. The role of banks in the management of genetic resources and the conservation of endangered species is particularly noticeable in the last decade. Most cryobanks focus on the cryopreservation of gametes (primarily sperm) and embryos. Their main goal is to produce offspring using reproductive technologies, which include artificial insemination, in vitro fertilization and embryo transfer. The discovery of the phenomenon of reprogramming somatic cell nuclear allowed expanding the range of forms of biological material in programs for cryopreservation. Creating cryobanks of somatic cells as donors of nuclei for cloning considered an auxiliary instrument for the preservation and improvement of the gene pool of farm animals and poultry. To obtain viable cryopreserved cell lines very small amount of biopsy material, including that of dead animals, is sufficient, but such lines contain the complete genome and proteome. In contrast to germ cells, embryos and generative tissues, the cryopreserved somatic cells after repeated thawing are capable to regenerate, i.e. almost infinitely may serve as a source of biomaterial for use in assisted reproductive technologies and biological research, including retrospective reconstruction. Furthermore, due to the small size the somatic cells are more resistant to cryopreservation. This review also provides a brief description of the principles and history of cloning. The advantages of the use of different cell types as karyoplasts are discussed. In particular, almost all types of cells (e.g. embryonic cells, mammary cells, cumulus, granulosa, oviduct, liver, fibroblasts, white blood cells and embryonic stem cells) can be used for the production of cloned animals, but the cloning efficiency depends significantly on the type of cells. Aiming embryo development and birth of live offspring, the fetal fibroblasts as donors of nuclear material for cloning are most effective. Alternatively, the stem cells may be a source of the nuclei. Stem or progenitor cells (i.e., stem, determined to differentiate in specific type cells) are easier reprogrammed than terminally differentiated cells. Also when stem cells nuclei are used as karyoplasts the number of cloned embryos significantly increased. The advances in interspecific cloning as a strategy for restoration of rare and endangered species are discussed. Numerous examples show that somatic cells can be considered the most promising material for the recovery of animal genetic resources of different types. Particularly from 1997 to 2012 using the differentiated somatic cells domestic and wild animals of different species were obtained such as sheep, mice, cows, goats, pigs, guar, mouflon, domestic cat, rabbits, mule, horse, rat, wildcat, dog, banteng, ferret, wolves, buffalo, deer, mountain goat, camel, coyote. Cattle are still the leader in the production of cloned offspring with the efficacy 10% on average, and in some cases up to 25%, while for most other animals it does not exceed 1%. Under controlled conditions in farms with good management, the productivity of clones should vary only within the remaining natural variability and mitochondrial genetic variability due to cloning technology.
Keywords: somatic cells cryobanks, cloning, biodiversity, animal genetic resources.
Extinction of many species is irreversible and is a part of the natural evolution. People activities, particularly uncontrolled hunting and fishing, destruction of environment, along with animal competition for food and terri-
tory influence this process making extinction much faster comparing to speciation (1). Changing demands of the market and the intensification of agriculture have also increased tendency to reduction of biodiversity of domestic animals. In agriculture small farms are gradually replaced by large commercial enterprises. Recent reproduction technologies, an unlimited transfer of genetic material, breeding programs implemented by national and international companies lead to dominance of certain livestock breeds (2). According to FAP reports, about 20% of cattle, goats, pigs, horses and poultry breeds in the world are currently under threat of disappearance. Many breeds have become extinct during past few years with their genetic characteristics lost irreversibly (3). With the view to bio-, environmental and food safety it is essential to maintain biodiversity and alternative and potentially useful genes in the gene pool (4). In 2007 109 countries have approved Global Plan of Action for Animal Genetic Resources due to understanding this problem (5).
Obviously both wild and domestic animals should be best preserved in situ, i.e. in their natural habitat meaning nature or commercial farming with specific technology used for each breed. This is costly as the extensive infrastructure and management are required. Besides, in case of small population and necessity to keep up an adequate genetic diversity this approach could be insufficient (2). Banking of genetic recourses allows solving these problems additionally to in situ preservation (6−8).
The role of genetic resource banks, which provide collection, processing and storage of biomaterial, in the management and conservation of endangered species is particularly noticeable in the last decade (9). Under correct usage these recourses are enough to keep up current genetic diversity in the populations and allow their reproduction in the future using biotechnology (10). A core problem in creating such banks is to determine the quantity and type of preserved genetic material. Most cryobanks focus on cryopreservation of the gametes (primarily sperm) and the embryos, being targeted to offspring reproduction by means of assisted reproductive technologies, including artificial insemination, in vitro fertilization and embryo transfer (11). Somatic cell nuclei reprogramming allows expanding the range of biological material used in programs for cryopreservation. Cryobanking of somatic cells as the nuclei donors for cloning is recently considered the additional approach to preservation and improvement of agricultural animals and poultry gene pools (12).
Cultivation and freezing somatic cells allow to obtain the hundreds of millions of cells from an individual animal (and then preserve them for many years) that is similar in number to the culture of microorganisms. Specific complex media, which consist of amino acids, vitamins, sugars and blood serum containing sets of growth factors, are developed for effective somatic cell cultivation. The air CO2 concentration and the temperature optimal for cultivation are specified. Developed techniques of stable line cultures allow cultivating cells for a dozen passages with no changes in karyotype and all traits of normal cells (13).
Unlike the gametes and embryos the somatic cells are smaller and, therefore, more resistant to cryopreservation. After decades of application and improvement the cryopreservation became a routine procedure for most cell types. It includes cell isolation from tissue, cultivation, obtaining primary cell culture, cell biomass accumulation, freezing and storing in liquid nitrogen (13).
In cryobanks the samples should be stored at the temperature below -146 °C, providing their high chemical and physical stability. Therefore, the stored biological material is valuable both for conservation of genetic resources ex situ and future research projects and investigations (14). Very small amount of biopsy material, including that of dead animals, is sufficient to obtain the
viable cryopreserved cell lines, but such lines contain the complete genome and proteome. In contrast to gametes, embryos and generative tissues, the cryopreserved somatic cells are capable to regenerate after repeated thawing, i.e. almost infinitely may serve as a source of biomaterial for use in assisted reproductive technologies and biological research and manipulations, including retrospective reconstructions (9, 15).
The activities of Frozen Ark, the international consortium (16), and its members, particularly the Can Diego Zoo (California, USA) (17), LaCONES (India) and Genome Resource Bank (CGRB) for Korean Wildlife (Seoul National University) (10), clear demonstrate the role of cryobanks in preservation of genetic resources of the domestic animals and wildlife. Creating somatic cell and tissue banks is a part of national programs of genetic resource conservation in Canada, Brazil, Chine, Germany, Poland, Spain, Turkey (10, 15, 18−23). Noteworthy results were achieved when the somatic cell banks and cloning technology were used to preserve the native Anatolian breeds of domestic animals (23).
Cloning means an excision of nucleus from mature oocyte and its replacement by the donor nucleus from somatic cell. The donor nucleus influenced by different ooplasmic factors is undergone the epigenetic reprogramming. As a result the differentiated donor nucleus becomes active and initiates embryo development instead of somatic cell division (24).
Cloning was first suggested in 1938 by H. Spemann who showed the plurypotency of cell nuclei until 16 cell stage in salamander embryo (25), but the experimental nuclei transfers in mammals were reported much later in the 1980s. As mammalian zygotes are small in size, it causes technical difficulties in manipulations. Nevertheless, first reports about mouse cloning were dated 1981. In 1986 S.M. Willadsen reported the first successful nuclear transfer in sheep (26). Cloned sheep was obtained by the microsurgical enucleation of oocytes at MII with further fusion to 8 and 16 cell blastomeres. After the success with early blastomeres there were attempts to use cultivated animal cells in cloning. In 1996 in Scotland University K.H.S. Campbell et al. (27) used donor nuclei from blastocyst inner cell mass. In these experiments two lambs, Megan and Morag, were born that became a crucial step towards obtaining clones using somatic cells of an adult animal.
The first cloned progeny via somatic cell nuclei transfer in mammals was obtained in the same university in 1997 (28). The birth of cloned sheep Dolly generated great scientific interest and contributed to further numerous studies in cloning other animal species by means of somatic cell nuclei transfer.
A number of wild and domestic animal species have been recently cloned using differentiated somatic cells (28−49) (Table).
First cloned progeny in different animal species
Year I Animal species I References
1997 Sheep Овцы A.E. Schnieke et al. (Great Britain) (28)
1998 Mice T. Wakayama c et al. (USA) (29)
1998 Cows J.B. Cibelli et al. (New Zealand) (30)
1999 Goats A. Baguisi et al. (Japan) (31)
2000 Pigs I.A. Polejaeva et al. (Great Britain) (32)
2000 Guar R.P. Lanza (USA) (33)
2001 Mouflon P. Loi et al. (Italy) (34)
2002 Domestic cat T. Shin et al. (USA) (35)
2002 Rabbits P. Chesne (Chine) (36)
2003 Mule G.L. Woods et al. (USA) (37)
2003 Horse C. Galli et al. (Italy) (38)
2003 Rat Q. Zhou c соавт. (France, Chine) (39)
2004 Wild cat M.C. Gomes с соавт. (USA) (40)
2005 Dog B.C. Lee с соавт. (Korea) (41)
2005 Banteng M.J. Sansinena с соавт. (USA) (42)
2006 Ferret Z. Li с соавт. (Chine, USA, France) (43)
2007 Wolf M.K. Kim с соавт. (Korea) (44)
2007 Buffalo D. Shi с соавт. (Chine) (45)
2007 Red deer D. K Berg с соавт. (New Zealand) (46)
2009 Mountain goat J. Folch с соавт. (Spain) (47)
2010 Camel N.A. Wani с соавт. (UAE) (48)
2012 Coyote I. Hwang с соавт. (Korea) (49)
Almost any cell types can be used in animal cloning (12). There are reports on cells of embryos (50), mammary glands, cumulus, granulosa, oviduct, liver (29, 51−55), fibroblasts (56), leukocytes (57) and embryo stem cells (58) used as nuclei donors, but cloning efficacy essentially depends on the cell type. In view to successful embryonic development and the birth of viable animal the fetal fibroblasts are the most beneficial donors of nuclei under cloning. For these cells a low level of mutations and high proliferation are characteristic (12). However, sometimes there are no reasons and chance to obtain fetal biomaterial, when somatic cell banks are created, and then the tissues of adult animals could be the cell sources, mainly skin, muscles and cartilage. Fresh, stored at +4 °C for not more than 2 weeks or frozen biomaterial is suitable (59). A disadvantage of such cells is their lower capability to reprogramming and embryo development compared to fetal fibroblasts (60, 61).
The stem cells are recently considered the alternative source of nuclei for cloning. These cells are in each organ of adult animals providing structural and functional homeostasis. A proliferative ability and higher plasticity are the valuable traits of stem cells compared to differentiated somatic cells (62). Experiments on the mice neural stem cells showed an easier reprogramming of stem or progenitor cells comparing to differentiated cells, moreover, when stem cell nuclei were used as karyoplast the number of cloned embryos significantly increased (63). Nowadays, mesenchymal stem cells are considered the most attractive source of nuclei for cloning (64−66).
The adult animal cells significantly increase a potential of cloning technology in conservation of animal and poultry genetic resources and also in breeding. Cloning adult animals allows to replace the genetic selection by a phenotypic selection. Chromosomal gene combination under cloning remains unchanged thus not only the additive gene effects can be used. Under controlled conditions in farms with effective management the productivity of cloned animals should differ only within a residual natural variability and also due to mitochondrial genetic variability occurred because of used cloning technology. As a result, one generation in the herd is enough to reach the best productivity. In that connection the selection of animals with high lifetime productivity is particularly important (22).
Despite the recent impressive successes in cloning, its efficacy remains extremely low with the high level of embryo abnormalities and a decreased viability of the offspring (67, 68). Cattle still remains the leaders among cloned species with an average 10% frequency of the offspring birth, being even 25% in some cases, in contrary to most other animal species with not more than 1% frequency as a rule. So, by creating somatic cell and tissue banks now we provide biomaterial for future applying when improved cloning technology will allow its effective use (69).
A search for universal cytoplast to be used in somatic cell nuclei transfer is an important point of cloning. These experiments became the most relevant in connection with programs of wildlife genetic resource conservation when obtain-
ing autogenic cytoplasts for obvious reasons is impossible or difficult. The oocytes used for interspecial cloning should meet special requirements. Technology of cytoplast processing should not be expensive or difficult, and cytoplast should be capable to reprogram the somatic cells of another species and support the embryo development of an interspecial cytohybrid.
In 1999 T. Dominko et al. (70) first demonstrated the capability of cattle oocyte cytoplasm to reprogram the nuclei of somatic cells of other animal species. After the transfer of nuclei from sheep, pig, monkey or rat skin cells to MII enucleated cattle oocyte the cytoplast and xenogenic karyoplast joined. In further experiments cattle oocytes were used as cytoplasts in transfer of somatic cell nuclei of pigs (71), koala (72), antelope, goat (73), horses (74), black bear (75), mountain antelope (76), hens (77), yak and dog (78), and buffalo (79). These cytoplasts are preferable because of their low cost (due to isolation from ovaries of slaughtered animals) and easy cultivation which allows 90% maturation. Moreover, the technology of oocytes and embryos cultivation in this species is currently considered the most improved.
In 2000 the cloning of gaur, being on the edge of extinction, was first reported. In this experiment the nuclei of adult male gaur fibroblasts were injected into enucleated cow oocytes, then 44 in vitro cultivated embryos were transplanted to 32 cows and a calf was born alive (33).
Interspecial cloning of banteng (Bos javanicus) is good example of species revivalism. For recent 15−20 years it decreased in number by 85%. In 2003 in USA the measures have been taken to preserve this rare species. Because of absence of autogenic oocytes the interspecial transformation was impossible, so the cow oocytes were used as recipients in transfer of the nuclei from adult ban-teng male and female skin fibroblasts. The biomaterial was received from the San Diego Zoo’s Center for Reproduction of Endangered Species (CRES), where the tissues of endangered animals are stored. In the experiment two calves were born after transplantation of 30 balstocysts to surrogate mother cows (42).
Intriguing progress has been achieved on the home sheep and their wild relatives, especially in the European mouflon. Somatic cell nuclei of adult mouflon female found died in a pasture were injected into enucleated oocytes of domestic sheep, and the recipient sheep were transplanted with embryos, resulting in alive offspring birth. In 2001 (34) the reproductive cloning has been successfully applied to the vanishing species Ovis musimom. In the experiment the dead females were a source of genetic material and the efficacy was much higher than at Dolly cloning.
In Spain in 2009 a cloned cub of extinct subspecies Capra pyrenaica pyrenaica was born after the bucardo somatic cells were transferred into domestic sheep oocytes and the surrogate mothers of other subspecies or hybrids from crossing domestic and wild goats were transplanted with the embyos. Of 439 obtained embryos the 57 ones were implanted into surrogate uterus, and one bucardo female cub was born but died 7 minute after birth because of breathing problems (47).
A potential of cloning technology discussed hereinabove is based on its current achievements. Nevertheless, it is still unclear whether the cloning technology could be improved soon to optimize the expenses for using nuclei of adult animal somatic cells and the efficiency of the procedure at an acceptable level.
Thus, cryobanking of somatic cells as nuclei donors in cloning is regarded as an assisted technique for conservation and improving gene pools of agricultural animals and poultry. In contrast to gametes, embryos and generative tissues the cryopreserved somatic cells are capable to regenerate after repeated thawing, i.e. almost infinitely may serve as a source of biomaterial for use in
assisted reproductive technologies and biological research, including revivalism and retrospective reconstructions. Besides, the somatic cells are more resistant at cryoconservation due to smaller size. Almost any cells could be used for cloning, but the cell type is essential for efficiency of the procedure. The highest results of embryo development and offspring birth are reached when fetal fibroblasts are used as nuclei donors. Stem cells are an alternative nuclei source. The domestic and wild animals of different species such as sheep, mice, cows, goats, pigs, guar, mouflon, domestic cat, rabbits, mule, horse, rat, wildcat, dog, banteng, ferret, wolves, buffalo, deer, mountain goat, camel, coyote have been obtained by cloning. Cattle still remains the leader in cloning due to offspring output of 10% and sometimes up to 25%, while in other species the cloning efficiency is still not more than 1%. If cloning are used, the best productivity can be reached in commercial herd during one generation, but practical expansion of cloning technology, particularly use of cryopreserved biological material, depends largely on whether there would be the acceptable relationship between the cost of implementation and economical impact.
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