www.elsevier.comrlocateranireprosci
Current state in biotechnology in canine and feline
reproduction
W. Farstad
)Department of Reproduction and Forensic Medicine, Norwegian School of Veterinary Science, P.O. Box 8146 Dep., N-0033 Oslo, Norway
Abstract
Biotechnology has proceeded much further in cats than in canines, although the pregnancy rate
Ž . Ž .
after in vitro maturation IVM , IVC and embryo transfer ET is still relatively low. The use of AI with frozen–thawed semen as a breeding tool to overcome breeding incompatibility or to preserve male genetic material has been limited in felines in contrast to the situation in domestic dogs and foxes. In many research scenarios and endangered felid species programs, the in vitro production of feline embryos with subsequent transfer has complemented the use of AI.
Improve-Ž .
ment of IVM, in vitro fertilization IVF and embryo culture coupled with ovarian tissue grafting, cryobanking of follicles, oocytes, semen, or embryos, with subsequent ET into surrogate females, may render this technology feasible for use in endangered wild felids. In canines, reliable systems for in vitro production of embryos, embryo cryopreservation and transfer are yet to be developed. The refinement of invasive fertilization techniques, such as intracytoplasmic sperm injection
ŽICSI , may eventually provide a tool for removal of recipient oocyte nuclei and transfer of.
selected embryonic or somatic cell donor nuclei into domestic cat ooplasm, thereby providing a tool for genetic modification, or for preservation of valuable genetic material. q2000 Elsevier
Science B.V. All rights reserved.
Keywords: Canine; Feline; Artificial insemination; In vitro fertilization; Embryo transfer
1. Introduction
Ž . Ž .
Domestic cats Felis catus and dogs Canis familiaris primarily serve as compan-ion animals, and breeding has not been subject to planning on a large-scale basis as in
)Tel.:q47-22964855; fax:q47-22597081.
Ž .
E-mail address: wenche.farstad@veths.no W. Farstad .
0378-4320r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved. Ž .
other domestic animals. Most breeding is within small kennels with a small number of breeding animals, with the exception of large colonies of cats and dogs bred exclusively for biomedical research. In dogs, the export and import of semen and live breeding animals have shown a steady increase, and semen banks have been established both in
Ž .
research institutions and by private companies Farstad, 1996 . In the cat, however, exchange of breeding animals occurs within laboratory animal research institutions, but commercial initiatives relating to trade with frozen semen are scarce. The semi-domestic
Ž . Ž .
fox breeds, the red fox Vulpes Õulpes and the blue fox Alopex lagopus have been
farmed for pelts mainly in Northern America, the Nordic countries, Russia, the Baltic
Ž .
states and Poland since the early 1900s Nes et al., 1987 , and in this context planned breeding has been carried out to a larger extent than in dogs and cats. Also, international trade with live breeding animals was extensive during the 1960s and 1970s, and during the last 5 years, frozen silver fox semen has been exported from Norway to Canada with
Ž .
the birth of live pups Fougner, 1999, personal communication .
There has been relatively limited interest in conserving the wild members of the canid family by means of assisted reproduction — in many cases because most of them reproduce well both in the wild and in captivity, but also because progress in reproduc-tive biotechnology has encountered major problems particularly concerning in vitro
Ž models for female gametes and embryos. At present, both the gray wolf, red wolf C.
. Ž . Ž .
rufus , Mexican wolf C. lupus baileyi , Egyptian wolf Lycaon pictus , Ethiopian wolf ŽC. simensis , South American Savannah dog Speothos. Ž Õenaticus , maned wolf Chry-. Ž
. Ž .
saocon brachyarus and two fox species: the San Joaquin kit V. macrotis and the
Ž .
Northern swift fox V. Õelox hebes , are considered to be threatened by extinction
ŽGottelli et al., 1994; Goodrowe et al., 1998; IUCN 1996; CITES, 1997, 1998 . In.
Ž .
Scandinavia, the wild polar fox A. lagopus is considered vulnerable. Thus, with
limited space in the wild and in zoological institutions, the need for strategies involving multidisciplinary action for enhancing conservation of these species is increasing rapidly.
Most of the 36 wild species of felids are classified as threatened, vulnerable or
Ž .
endangered Nowell and Jackson, 1996 , maybe with the exception of the Northern
Ž .
European lynx Lynx lynx , which is again hunted, although by restricted licences, in Norway and Sweden. In wild cats, research for biotechnology development is well underway with the establishment of conservation programs in which assisted
reproduc-Ž .
tion plays an important part Wildt et al., 1992 . Research on maturation, fertilization Ž .
and embryo development in vitro, as well as embryo transfer ET and cryopreservation Ž
has increased rapidly during the last decade in domestic cats Goodrowe et al., 1988, 1989, 1991; Johnston et al., 1989; Donoghue et al., 1992; Luvoni and Oliva, 1993; Pope et al., 1993, 1994, 1997, 1998; Schramm and Bavister, 1995; Wood and Wildt, 1997;
. Wood et al., 1995; Wolfe and Wildt, 1996; Luvoni et al., 1997; Howard, 1999 as well
Ž
as in wild felids Donoghue et al., 1993, 1996; Howard et al., 1992, 1997a; Swanson et .
felines, and in the following, a review on recent progress will be given for each of these carnivore families.
2. Canines
Canines are monoestrous. Seasonality is not obvious in most breeds of dogs, except for the Basenji, in which females experience estrus during the autumn in the northern
Ž . Ž .
hemisphere. The blue A. lagopus and red foxes V. Õulpes are seasonal with their
breeding season during January–March. Ovulation occurs 1–2 days after the preovula-tory LH peak at the beginning of estrus in both dogs and foxes. In bitches and vixens, preovulatory luteinization of follicles occurs, exposing oocytes to increasing concentra-tions of progesterone, as opposed to the situation in many other domestic mammals, where estrogen dominates the preovulatory follicular environment. In most mammals, ovulation of the oocyte occurs when the oocyte has reached the metaphase of the second meiotic division. In canines, the oocyte is ovulated at the beginning of the first meiotic division, and the germinal vesicle is broken down shortly after ovulation. Subsequent
Ž
stages of oocyte maturation occur in the oviduct Holst and Phemister, 1971; Farstad et .
al., 1989 .
2.1. Oocyte maturation, fertilization and embryonic deÕelopment in Õitro
Canine oocytes may resume meiosis spontaneously in vitro using adaptations of
Ž .
bovine and porcine in vitro maturation IVM techniques, although at a much lower rate and efficiency than most other domestic animal oocytes. In canids, IVM has shown limited success with maturation rates varying from 0% to 58% for oocytes matured to
Ž .
Metaphase I, Anaphase I and Metaphase II MIrAIrMII ; maturation is usually around
Ž . Ž
20% MII , in a variety of different culture systems and media Mahi and Yanagimaci, 1976; Robertson et al., 1992; Nickson et al., 1993; Yamada et al., 1992, 1993; Bolamba et al., 1997; Hewitt and England 1997, 1998a, 1999a; Hewitt et al., 1998; Theiss, 1997;
.
Metcalfe, 1999 . Most oocytes used for IVM experiments in the dog have been collected from random sources, usually from animals undergoing ovariohysterectomy. Hence, oocytes from prepubertal, anestrous, luteal phases of pregnant and non-pregnant animals, as well as proestrous and estrous females have been used with no apparent effect of the
Ž
stage of estrous cycle Nickson et al., 1993; Hewitt and England, 1997; Theiss, 1997;
. Ž
Metcalfe, 1999 , whereas the age of the donor animal Nickson et al., 1993; Hewitt and
. Ž
England, 1998a , oocyte size Theiss, 1997; Hewitt and England, 1998a; Srsen et al.,
. Ž .
1998 and nuclear and cumulus morphology Nickson et al., 1993 all influence IVM rates. In foxes, the IVM of ovarian oocytes, collected either from preovulatory or
Ž anestrus follicles, have resulted in maturation rates similar to those in the bitch i.e.,
. Ž .
80% — 100 GVBD, 25% MII Krogenæs et al., 1993; Wen et al., 1994 . Recently,
maturation rates to MII have been improved for blue fox oocytes collected from
Ž . Ž .
anestrous animals 40% MII Srsen et al., 1998 . Canine oocytes may undergo IVM in
Ž .
grafting to host ovaries of SCID mice. Graft establishment and some follicular recruit-Ž ment occurred, even though the production of antral follicles was not obtained
Met-.
calfe, 1999 . A refinement of this technique may enable the use of ovaries from valuable animals for further production of oocytes posthumously.
Canine embryos have been produced after fertilization in vitro of in vivo matured ŽRenton et al., 1991; Farstad et al., 1993a , and from in vitro matured oocytes, but in the.
Ž
latter development beyond the eight-cell stage has not been reported Yamada et al., .
1993; Metcalfe, 1999 . An in vitro ‘‘block’’ to development has been described for
Ž . Ž
many species in which in vitro fertilization IVF has been attempted for a review on developmental ‘‘block’’ in vitro of mouse, hamster, sheep and cow embryos, see
. McGinnis and Youngs, 1992; Sparks et al., 1992; for cat: Swanson et al., 1996a . The maternal embryonic transition constitutes a critical phase of embryo development. In foxes and dogs, structural studies and cultivation with 3H-uridine, indicate that activa-tion of the embryonic genome occurs at the six- to eight-cell stage in foxes and the
Ž .
eight-cell stage in dog embryos Farstad et al., 1993b; Bysted and Greve, 2000 . The scarcity of reports in the literature of attempts to modify the culture conditions in vitro for IVM-derived embryos after the eight-cell stage may indicate that some difficulties have been encountered in propagating development past this stage, but too little information is available to conclude that such an in vitro block exists in dog oocytes. To date, no reports of production of live young after IVF from either in vivo- or in vitro matured dog or fox oocytes exist in the literature.
2.2. Sperm treatment, cryopreserÕation and assisted fertilization
The in vitro capacitation of canine sperm may be achieved in canine capacitation
Ž . Ž
medium Mahi and Yanangimaci, 1976 or in modified Tyrode’s solution Farstad et al., .
1993a,b; Hewitt and England, 1999b . Calcium ionophore A23187 can promote capaci-2q Ž
tation and the acrosome reaction in a similar manner as Ca in vitro Szasz et al., 1997;
.
Hewitt and England, 1998c . The reports on IVF rates in dogs or foxes are few, but cleavage rates of 5–20% and pronuclear formation in 20–37% of oocytes have been
Ž
reported Farstad et al., 1993a,b; Nickson et al., 1993; Yamada et al., 1993; Metcalfe,
. Ž .
1999 . Intracytoplasmic sperm injection ICSI has been attempted with chilled dog sperm, with the formation of male pronuclei in 8% of oocytes, but no cleavage occurred ŽFulton et al., 1998 ..
The cryopreservation of dog and fox semen has been frequently reviewed, and a variety of freezing regimens, extenders and thawing protocols for dog and fox semen
Ž .
have been published England, 1993; Farstad, 1996; Rota, 1998 . Recently, modifica-tions of the commonly used TRIS egg yolk extender by the addition of Equex STM
paste improved post-thaw survival of dog sperm during incubation at 388C and produced
Ž . Ž
an overall pregnancy rate after vaginal or intrauterine IU AI of 84% Rota et al., 1997, .
1999 . Differences between canine species with respect to cooling tolerance may exist,
Ž . Ž .
since freezing trials with blue foxes A. lagopus and red wolves C. rufus have
resulted in a significant reduction in the percentage of intact acrosomes after freezing
Ž .
dog sperm, which may also be usable for the assessment of sperm function in vitro for Ž
other canines Hay et al., 1997; Hewitt and England, 1998b,c; Mayenco-Aguirre and .
Peres-Cortez, 1998, Strom Holst, 1999 . Red wolf sperm bind to domestic dog oocytes
¨
ŽGoodrowe, 1999, personal communication ..
2.3. Artificial insemination and ET
IU artificial insemination may be carried out non-surgically using either endoscopic Ž
visualization or transcervical catheterization, or surgically by laparoscopy for review, .
see Farstad, 2000 . Results in foxes and dogs using IU non-surgical AI are good, and Ž
both birth rates and litter sizes approach those of natural mating see reviews Farstad, .
1996, 1998 . The ET of in vivo-derived embryos has been carried out surgically both in Ž
the silver fox and the dog resulting in live young, but with low success rates Kinney et .
al., 1979; Tsutsui et al., 1989; Jalkanen and Lindeberg, 1998 . Recently, ET has been carried out in the blue fox, using the IU catheter developed for artificial insemination in
Ž .
foxes Lindeberg, 1999, personal communication . To date, the birth of live young from cryopreserved canine embryos has not been reported. However, in the blue fox, freezing of embryos recently resulted in the observation of implantation sites in naturally
Ž .
synchronized recipient females after ET Lindeberg, 1999, personal communication . The refinement of freezing regimens, improvement of donor-recipient synchronization, in vitro handling of embryos and transfer techniques may soon render both cryobanking of embryos and ET feasible in foxes.
3. Felines
3.1. Oocyte maturation
Generally, cats are seasonally polyestrous carnivores with sexual activity during the months of increasing day length, and sexual inactivity during the months of declining
Ž .
day lengths. Contrary to canines and most other domestic animals, cats are usually reflex ovulators, i.e. oocytes are ovulated 24–48 h after the post-coital LH release. The
Ž .
oocytes are ovulated as secondary oocytes in metaphase II. Goodrowe et al. 1988 first demonstrated that unovulated follicular oocytes after IVF were able to sustain develop-ment to term with the birth of live kittens. IVM rates are relatively high in cat oocytes
Ž40–60% depending on the quality of the oocyte and the type of hormonal supplemen-.
tation. The stage of the estrous cycle and supplementation of maturation media with Ž
gonadotrophins Goodrowe et al., 1991; Schramm and Bavister, 1995; Wood et al.,
. Ž
1995; Pope et al., 1997 and quality of the cumulus oocyte complex Wood and Wildt, .
1997 influence in vitro development. The highest incidence of MII can be expected after 40–48 h of IVM, similar to the time period from mating to ovulation in the queen ŽGoodrowe et al., 1989 . However, other studies have found that most oocytes reach MII. within the first 24 h of IVM, and insemination at 40 h or later does not result in
Ž .
Ž
felines than in canines, and maturation occurs more rapidly 40–60% MII, 24 h IVM vs. .
0–58% AIrMIrMII, 48–72 h IVM, respectively , but IVM rates are still lower than in
Ž .
most farm animal IVM systems )80%, 24 h IVM . IVM has also been successful in
Ž .
some non-domestic felids Johnston et al., 1991 .
3.2. Sperm treatment and assisted fertilization
The quality of ejaculated sperm differs within felid species. Some breeds with low genetic variability have a high incidence of teratospermia and high number of sperm
Ž . Ž .
with acrosomal defects, such as the cheetah Acinonyx jubatus Wildt et al., 1992 . The
structural mechanisms relating to the acrosome and functional defects in protein phosphorylation of some wild feline sperm may be the cause of decreased sperm
Ž .
function Goodrowe, 1999, personal communication . Homologous or heterologous zona binding systems and oocyte penetration assays have been developed for feline sperm ŽGoodrowe and Hay, 1993; Swanson et al., 1998; Nelson et al., 1999 . Fertilization rates. after in vitro fertilization of domestic cat oocytes varies between 40% and 50% of in
Ž
vitro matured and 60–80% of in vivo matured oocytes Pope, 1999, personal communi-.
cation . In vitro fertilization has been successful in the domestic cat in terms of Ž
production of both embryos and live offspring Goodrowe et al., 1989; Hoffert et al.,
. Ž )
1997 . In a few non-domestic felids, such as the tiger Panthera tigris and Indian
Ž . Ž
Desert cat F. silÕestris , offspring have been obtained Pope et al., 1989; Donoghue et .
al., 1990; for review, see Howard, 1999 .
Lately, blastocysts have been obtained from in vivo matured oocytes collected from gonadotrophin stimulated domestic queens, fertilized in vitro by any of the following: Ž .1 co-incubation with sperm, 2 subzonal insemination SUZI or 3 ICSI Pope et al.,Ž . Ž . Ž . Ž
. Ž
1998 . Earlier attempts at comparing SUZI and ICSI were in favor of SUZI Pope et al., .
1995 , but improvements in sperm injection technique and visualization of ooplasm by centrifugation of oocytes improved results considerably in favor of ICSI. ICSI is the most invasive of the assisted fertilization techniques: it allows fertilization with
immo-Ž .
bile teratogeneic sperm, and also enables fusion between nuclei at different stages of development. Thus, refining methods for injection of sperm or other DNA containing material into the oocyte may spur the development of nuclear transfer techniques in felids, and thereby provide the possibility for genetic modification, as well as for conservation of nuclear material. Cat ooplasm could be a potential host for somatic cell nuclei from endangered species of felids, as suggested by the bovine model, which demonstrated that bovine oocyte cytoplasm supports embryo development of nuclear
Ž .
transfer produced embryos from many species Dominko et al., 1999 .
3.3. Embryo culture inÕitro
In vivo matured oocytes readily develop to the blastocyst stage after in vitro fertilization and culture. The developmental rate of in vivo matured in vivo fertilized
Ž .
embryos to the morula stage in TCM 50–90% , and the rate of blastocyst formation
Ž .
was 50–66% mean rate 64.7% depending on the developmental stage of the
ŽKanda et al., 1995 . Blastocysts have been produced by IVC of in vitro matured and. Ž IVF cat oocytes, and the rate of blastocyst formation varied between 10 and 50% Wolfe and Wildt, 1996; Wood and Wildt, 1997; Pope et al., 1997; Freistedt et al., 1999;
.
Swanson et al., 1999 . Live kittens have been born after transfer of embryos produced
Ž .
by complete in vitro generation, i.e. IVM, IVF and IVC Pope et al., 1997 .
Until recently, a high percentage of felid embryos produced in vitro experienced a developmental block at the morula to blastocyst stage, i.e. somewhat later than the in
Ž
vitro block observed in other mammals Donoghue et al., 1990; Johnston et al., 1991; .
Roth et al., 1994; Swanson et al., 1996b; Hoffert et al., 1997 . A difference in
Ž .
metabolism glycolysis was demonstrated between in vivo and IVM cat oocytes that may partially explain why IVM oocytes may have developmental difficulties after IVF
Ž .
was compared with in vivo matured oocytes Spindler and Wildt, 1999 . A recent study showed that both supplementation of cysteine to the maturation medium and reduction of the O atmosphere significantly improved in vitro development to the blastocyst stage2 ŽPope et al., 1999 . Thus, as in bovine IVF, in vitro matured cat oocytes do not develop. to blastocysts as readily as their in vivo matured counterparts, but the difference is no
Ž .
longer strikingly large due to improvements in culture conditions Swanson et al., 1998 . Results in the vicinity of 30–40% blastocysts from IVM oocytes vs. 40–50% from in
Ž .
vivo matured oocytes can be expected on day 7 Pope, 1999, personal communication .
3.4. Short- and long-term preserÕation of gametes, follicles and embryos
Reports on the of use of frozen semen for the exchange of feline genetic material has
Ž .
been limited Howard et al., 1997b . Cat semen may be chilled to 48C and stored for
Ž
24–48 h in a TesT buffer based on a trishydroxymethyl amino methane sulphonic acid
. Ž
buffer, Tes at pH 7.4, and subsequently used for AI or in vitro insemination Axner,
. Ž .
1998 . Buffers, such as TesT and Tris trishydroxy methylamino methane , have been
Ž .
used with 4% glycerol or dimethylsulphoxide DMSO and 20% egg yolk, yielding no
Ž .
differences between the tested extenders. High cryoprotectant concentrations i.e., 8%
Ž .
compromised cat sperm Nelson et al., 1999 . Pelleted freezing has often been the
Ž .
standard method Howard, 1986 . Freezing in straws has been found to be equal to
Ž .
freezing in pellets Wood et al., 1993 . A pregnancy rate of only 10% was obtained in Ž
cats after the use of frozen–thawed semen with vaginal deposition of semen Platz et al.,
. Ž .
1978 , and vaginal inseminations in wild felids have been unsuccessful Howard, 1999 . Offspring from IU laparoscopic AI with frozen–thawed semen have been obtained in
Ž . Ž . Ž .
ocelot F. pardalis , leopard cat F. bengalensis , cheetah Aci. jubatus , snow leopard ŽP. uncia , clouded leopard. ŽNeofelis nebulosa and tiger for review see, Howard,. Ž
. 1999 .
Cat oocytes collected from ovaries and exposed to up to 72 h in refrigerated storage
Ž .
matured to MII at normal rates 50–60% . Oocytes collected from ovaries that had been stored for 24 h developed to blastocysts, showing that cold storage of feline oocytes
Ž
does not compromise their ability to sustain development in vitro Wolfe and Wildt, .
DMSO, although the meiotic resumption rate was half the rate of unfrozen controls ŽLuvoni et al., 1997 . Isolated preantral ovarian cat follicles also have been cryopre-. served, showing that a small subpopulation of these follicles survive and are functionally
Ž .
intact after freezing with conventional cryoprotectants Jewgenow et al., 1998 . The first report on the birth of live kittens after ET of cryopreserved, in vivo-derived embryos
Ž .
was reported in 1988 Dresser et al., 1988 and later, from cryopreserved embryos
Ž .
produced in vitro from in vivo matured oocytes Pope et al., 1994 and after in IVM,
Ž .
IVF and IVC-derived cryopreserved cat embryos Pope et al., 1997 . The cryopreserva-tion of domestic cat embryos can be carried out in a variety of cryoprotectants. Modifications of freezing regimens for bovine and mouse embryos have provided
Ž .
promising results Pope et al., 1994, 1997; Swanson et al., 1999 .
3.5. Artificial breeding techniques
Artificial insemination in domestic cats has mostly been used in research, in which Ž
cats have served as model species. Laparoscopic insemination is often used Howard et al., 1992, 1997; Donoghue et al., 1993, 1996; Barone et al., 1994; Swanson et al.,
.
1996a . Deep vaginal insemination may be done in domestic cats by inserting a French
Ž .
Tom cat catheter as far as possible into the vagina see Axner, 1998 . A method for
´
non-surgical IU ET has been described, which may equally well be used for intrauterine
Ž . Ž .
AI Swanson and Godke, 1994 . Pregnancy rates are higher after IU laparoscopic AI
Ž .
both in domestic and captive wild cats see Axner, 1998; Howard, 1999 . The time of
´
insemination in relation to gonadotrophin stimulation and anaesthesia influences preg-nancy rates. The best time for AI when anaesthesia is used, is after ovulation has
Ž .
occurred Howard, 1999 .
ET has been carried out in both domestic and wild cats with both fresh and Ž
cryopreserved in vivo and in vitro-derived embryos Dresser et al., 1988; Pope et al., . 1989, 1994, 1997; Donoghue et al., 1990; Kanda et al., 1995; Swanson et al., 1998 . Surgical, laparoscopic and transcervical ETs have resulted in live offspring, albeit at a
Ž .
relatively low rate in terms of survival of transferred embryos Swanson et al., 1998 . Transfer to either the oviduct or the uterus has resulted in pregnancies. Lately, transferring 5–8 morulae or blastocysts per recipient improved overall pregnancy rate as
Ž .
well as pregnancy rate per recipient Swanson et al., 1999 .
4. Conclusion
in vitro production of embryos, embryo cryopresevation and transfer are yet to be developed, but progress has been significant during the last 2–3 years.
Acknowledgements
The author would like to express her sincere gratitude to Liisa Jalkanen and Heli Lindeberg at the University of Kuopio, Juankoski Fur Animal Research Station, Kuopio, Finland, for sharing yet unpublished data on non-surgical embryo transfer in blue foxes and trials with frozen fox embryos. The same goes also to the Danish group: Britta V. Bysted, Torben Greve and Poul Hyttel at the Royal Agricultural University, Copen-hagen, for providing submitted, yet unpublished material on genome activation in dog embryos. The author is also grateful to Karen L. Goodrowe, Toronto Zoo, Ontario, Canada, and Earle Pope, Cincinnati Zoo, OH, USA, who are both active in canine and feline reproductive biotechnology research, for valuable discussions.
References
Axner, E., 1998. Mating and artificial insemination in domestic cats. In: Simpson, G., England, G.C., Harvey,
Ž .
M. Eds. , British Small Animal Veterinary Association Manual of Small Animal Reproduction and Neonatology. BSVA, Cheltenham, UK, pp. 105–111, Chap. 10.
Barone, M.A., Wildt, D.E., Byers, A.P., Roelke, M.E., Glass, C.M., Howard, J.G., 1994. Gonadotrophin dose
Ž .
and timing of anaesthesia for laparoscopic artificial insemination in the puma Felis concolor . J. Reprod. Fertil. 101, 103–108.
Bolamba, D., Bordern-Russ, K.D., Durrant, B.S., 1997. In vitro maturation of dog oocytes derived from advanced preantral follicles in synthetic oviduct fluid: bovine serum albumin and fetal calf serum are not
Ž .
essentials. Biol. Reprod. 1, 96, Suppl .
Bolamba, D., Bordern-Russ, K.D., Durrant, B.S., 1998. In vitro maturation of domestic dog oocytes cultured in advanced preantral and early antral follicles. Theriogenology 49, 933–942.
Ž .
Bysted, B.V., Greve, T., 2000. Activation of the embryonic genome in the dog. Theriogenology 53 1 , 269,
Žabstr. ..
CITES, 1997. In: The Convention on International Trade of Endangered Species of Wild Flora and Fauna. 10th Meeting of the Conference of the Parties, Harare, Zimbabwe. .
CITES, 1998. In: The Convention on International Trade of Endangered Species of Wild Flora and Fauna. Cites-listed Species Database: Fauna. Chatelaine-Geneve, Switzerland. .ˆ `
Dominko, T., Mitalipova, M., Haley, B., Beyhan, Z., Memili, E., McKusick, B., First, N.L., 1999. Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species. Biol. Reprod. 60, 1496–1502.
Donoghue, A.M., Johnston, L.A., Seal, U.S, Armstrong, D.L., Tilson, R.L., Wolf, P., Petrini, K., Simmons, L.G., Gross, T., Wildt, D.E., 1990. In vitro fertilization and embryo development in vitro and in vivo in the
Ž .
tiger Panthera tigris . Biol. Reprod. 43, 733–744.
Donoghue, A.M., Johnston, L.A., Munson, L., Brown, J.L., Wildt, D.E., 1992. Influence of gonadotrophin treatment interval on follicular maturation, in vitro fertilization, circulating steroid concentrations and subsequent luteal function in the domestic cat. Biol. Reprod. 46, 972–980.
Donoghue, A.M., Johnston, L.A., Armstrong, D.L., Simmons, L.G., Wildt, D.E., 1993. Birth of a Siberian
Ž .
tiger cub Panthera tigris altaica following laparoscopic intrauterine artificial insemination. J. Zoo Wildl. Med. 24, 185–189.
Ž
gonadotrophin induction and its importance to successful intrauterine insemination in the tiger Panthera
.
tigris . J. Reprod. Fertil. 107, 53–58.
Dresser, B.L., Gelwicks, E.J., Wachs, K.B., Keller, G.L., 1988. The first successful transfer of cryopreserved
Ž .
feline Felis catus embryos resulting in live offspring. J. Exp. Zool. 246, 180–186.
Ž .
England, G.C., 1993. Cryopreservation of dog semen: a review. J. Reprod. Fertil. 47, 243–255, Suppl . Farstad, W., 1996. Semen cryopreservation in dogs and foxes. Anim. Reprod. Sci. 42, 251–260.
Farstad, W., 1998. Reproduction in foxes: current research and future challenges. Anim. Reprod. Sci. 53, 35–42.
Ž .
Farstad, W., 2000. Assisted reproductive technology in canid species. Theriogenology 53 1 , 175–186. Farstad, W., Mondain-Monval, M., Hyttel, P., Smith, A.J., Markeng, D., 1989. Periovulatory endocrinology
Ž .
and oocyte maturation unmated, mature blue fox vixens Alopex lagopus . Acta Vet. Scand. 30, 313–319. Farstad, W.K., Fougner, J.A., Andersen Berg, K., 1992. Species differences after artificial insemination with
Ž .
frozen semen in fox pure breeding. Norwegian J. Agric. Sci. 9, 115–121, Suppl. .
Farstad, W., Hyttel, P., Grøndahl, C., Krogenæs, A., Mondain-Monval, M., Hafne, A.L., 1993a. Fertilization
Ž .
in vitro of oocytes matured in vivo in the blue fox Alopex lagopus . J. Reprod. Fertil. 47, 219–226,
ŽSuppl. ..
Farstad, W., Hyttel, P., Grøndahl, C., Mondain-Monval, M., Smith, A.J., 1993b. Fertilization and early
Ž .
embryonic development in the blue fox Alopex lagopus . Mol. Reprod. Dev. 36, 331–337.
Freistedt, P., Stojkovic, B., Bonhoeffer, T., Braun, J., Wolf, E., 1999. In vitro production of domestic cat
Ž .
embryos using a modified IVP bovine system. Theriogenology 51, 285, abstr. .
Fulton, R.M., Keskintwepe, L., Durrant, B.S., Fayrer-Hosken, R.A., 1998. Intracytoplasmic sperm injection
ŽICSI for the treatment of canine infertility. Theriogenology 49, 366, abstr. .. Ž .
Goodrowe, K.L., Hay, M., 1993. Characteristics of zona binding ability of fresh and cooled domestic cat epididymal spermatozoa. Theriogenology 40, 967–975.
Goodrowe, K.L., Wall, R.J., O’Brien, S.J., Schmidt, P.M., Wildt, D.E., 1988. Developmental competence of domestic cat follicular oocytes after fertilization in vitro. Biol. Reprod. 39, 355–372.
Goodrowe, K.L., Howard, J.G., Schmidt, P.M., Wildt, D.E., 1989. Reproductive biology of the domestic cat with special reference to endocrinology, sperm function and in vitro fertilization. J. Reprod. Fertil. 39,
Ž .
73–90, Suppl. .
Goodrowe, K.L., Hay, M., King, W.A., 1991. Nuclear maturation of domestic cat ovarian oocytes in vitro. Biol. Reprod. 45, 466–470.
Goodrowe, K.L., Hay, M.A., Platz, C.C., Behrns, S.K., Jones, M.H., Wadell, W.T., 1998. Characteristics of
Ž .
fresh and frozen–thawed red wolf Canis rufus spermatozoa. Anim. Reprod. Sci. 53, 299–308. Gottelli, D., Sillero-Zubriri, C., Applebaum, G.D., Roy, M.S., Girman, D.J., Carcia-Moreno, J., Ostrander,
E.A., Wayne, R.K., 1994. Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Mol. Ecol. 3, 301–312.
Hay, M.A., King, W.A., Gartley, C.J., Leibo, S.P., Goodrowe, K.L., 1997. Canine spermatozoa-cryopreserva-tion and evaluaspermatozoa-cryopreserva-tion of gamete interacspermatozoa-cryopreserva-tion. Theriogenology 48, 1329–1342.
Hewitt, D.A., England, G.C., 1997. The effect of preovulatory endocrine events upon maturation of oocytes of
Ž .
the domestic bitch. J. Reprod. Fertil. 51, 83–91, Suppl. .
Hewitt, D.A., England, G.C.W., 1998a. The effect of oocyte size and bitch age upon oocyte nuclear maturation in vitro. Theriogenology 49, 957–966.
Hewitt, D.A., England, G.C.W., 1998b. The canine oocyte penetration assay; its use as an indicator of dog spermatozoal performance in vitro. Anim. Reprod. Sci. 50, 123–139.
Hewitt, D.A., England, G.C.W., 1998c. An investigation of capacitation and the acrosome reaction in dog spermatozoa using a dual fluorescent staining technique. Anim. Reprod. Sci. 51, 321–332.
Hewitt, D.A., England, G.C., 1999a. Influence of gonadotrophin supplementation on the in vitro maturation of bitch oocytes. Vet. Rec. 144, 237–239.
Hewitt, D.A., England, G.C., 1999b. Culture conditions required to induce capacitation and the acrosome reaction of canine sperm in vitro. Vet. Rec. 144, 22–23.
Hewitt, D.A., Watson, P.F., England, G.C., 1998. Nuclear staining and culture requirements for in vitro maturation of domestic bitch oocytes. Theriogenology 49, 1083–1128.
Holst, P.A., Phemister, R.D., 1971. The prenatal development of the dog. Preimplantation events. Biol. Reprod. 5, 771–779.
Howard, J.G., 1986. Semen collection, analysis and cryopreservation in nondomestic mammals. In: Morrow,
Ž .
D.A. Ed. , Current Therapy In Theriogenology. Saunders, Philadelphia, pp. 1047–1053.
Howard, J.G., 1999. Assisted reproductive techniques in nondomestic carnivores. In: Fowler, M.E., Miller,
Ž .
E.R. Eds. , Zoo and Wild Animal Medicine. Current Therapy 4. Saunders, Toronto, pp. 449–457, Chap. 61.
Howard, J.G., Donoghue, A.M., Barone, M.A., Goodrowe, K.L., Snodgrass, K., Starnes, D., Tucker, M., Bush, M., Wildt, D.E., 1992. Successful induction of ovarian activity and laparoscopic intrauterine
Ž .
artificial insemination in the cheetah. J. Zoo Wildl. Med. 23, 288, abstr. .
Howard, J.G., Roth, T.L., Byers, A.P., Swanson, W.F., Wildt, D.E., 1997a. Sensitivity to exogenous gonadotrophins for ovulation induction and laparoscopic insemination in the cheetah and clouded leopard. Biol. Reprod. 56, 1059–1068.
Howard, J.G., Roth, T.L., Byers, A.P., Swanson, W.F., Buff, J.L., Bush, M., Grisham, J., Marker-Kraus, L., Wildt, D.E., 1997b. Successful intercontinental genome resource banking and artificial insemination with
Ž . Ž .
cryopreserved semen in cheetahs. J. Androl. 55, Suppl. abstr .
IUCN, 1996. The 1996 IUCN Red List of Threatened Animals. IUCN Publications Service Unit, Cambridge, UK.
Ž .
Jalkanen, L., Lindeberg, H., 1998. Successful embryo transfer in the silver fox VulpesÕulpes . Anim. Reprod.
Sci. 54, 139–147.
Jewgenow, K., Blottner, T., Lengwinat, T., Meyer, H.H.D., 1997. New methods for gamete rescue from
Ž .
gonads of nondomestic felids. J. Reprod. Fertil. 51, 33–39, Suppl. .
Jewgenov, K., Penfold, L.M., Meyer, H.H.D., Wildt, D.E., 1998. Viability of small preantral ovarian follicles from domestic cats after cryoprotectant exposure and cryopreservation. J. Reprod. Fertil. 112, 39–47. Johnston, L.A., O’Brien, S.J., Wildt, D.E., 1989. In vitro maturation and fertilization of domestic cat follicular
oocytes. Gamete Res. 24, 343–356.
Johnston, L.A., Donoghue, A.M., O’Brien, S.J., Wildt, D.E., 1991. Culture medium and protein supplementa-tion influence in vitro fertilizasupplementa-tion and embryo development in the domestic cat. J. Exp. Zool. 257, 350–359.
Kanda, M., Oikawa, H., Nakao, H., Tsutsui, T., 1995. Early embryonic development in vitro and embryo transfer in the cat. J. Vet. Med. Sci. 57, 641–646.
Kinney, G.M., Pennycook, J.W., Schriver, M.D., Templeton, J.W., Kramer, D.C., 1979. Surgical collection
Ž . Ž . Ž .
and transfer of canine embryos. Biol. Reprod. 20 1 , 96A, abstr. Suppl. .
Krogenæs, A., Nagyova, E., Farstad, W., Hafne, A.L., 1993. In vitro maturation of blue fox oocytes and
Ž .
cAMP production in oocyte cumulus cell complexes. Theriogenology 39, 250, abstr. .
Luvoni, G.C., Oliva, O., 1993. Effect of medium-199 and fetal calf serum on in vitro maturation of domestic
Ž .
cat oocytes. J. Reprod. Fertil. 47, 203–207, Suppl. .
Luvoni, G.C., Pellizzari, P., Battochio, M., 1997. Effects of slow and ultrarapid freezing on morphology and
Ž .
resumption of meiosis in immature cat oocytes. J. Reprod. Fertil. 51, 93–98, Suppl. .
Mahi, C.A., Yanagimaci, R., 1976. Maturation and sperm penetration of canine ovarian oocytes in vitro. J. Exp. Zool. 196, 189–196.
Ž .
Mayenco-Aguirre, A.M., Peres-Cortez, A.B., 1998. Preliminary results of hemizona assay HZA as a fertility test for canine spermatozoa. Theriogenology 50, 195–204.
Metcalfe, S.S., 1999. Assisted reproduction in the bitch. Thesis for the degree of Master of Science, Monash University, Victoria, Australia, 160 pp.
McGinnis, L.K., Youngs, C.R., 1992. In vitro development of ovine embryos in CZB medium. Theriogenol-ogy 37, 559–569.
Nelson, K.L., Chrichton, E.G., Doty, L., Volenec, D.E., Morato, R.G., Pope, C.E., Dresser, B.L., Brown, C.S., Armstrong, D.L., Loskutoff, N.M., 1999. Heterologous and homologous capacity of cryopreserved felid
Ž .
sperm. A model for endangered species. Theriogenology 51, 290, abstr. . w
Nes, N., Einarsson, E.J., Lohi, O., 1987. Vare vakre pelsdyr og deres fargegenetikk. Our beautiful fur animals˚
x Ž .
and their color genetics Scientifur, Hillerød Denmark , 12.
biological methods for monitoring oocyte maturation and in vitro fertilization in bitches. J. Reprod. Fertil.
Ž .
47, 231–240, Suppl. .
Nowell, P., Jackson, P., 1996. In: Status Survey and Conservation Action Plan: Wild cats. IUCN, Gland, Switzerland, pp. 149–179.
Platz, C.C., Wildt, D.E., Seager, S.W.J., 1978. Pregnancy in the domestic cat after artificial insemination with previously frozen spermatozoa. J. Reprod. Fertil. 52, 279–282.
Pope, C.E., Gelwicks, E.J., Wachs, K.B., Keller, G.L., Maruska, E.J., Dresser, B.L., 1989. Successful
Ž .
interspecies transfer of embryos from the Indian Desert cat Felis silÕestris ornata to the domestic cat ŽFelis catus following in vitro fertilization. Biol. Reprod. 40 1 , 61, Suppl.. Ž . Ž . Žabstr ..
Pope, C.E., Keller, G.L., Dresser, B.L., 1993. In vitro fertilization in domestic and non-domestic cats including sequences of early nuclear events, development in vitro, cryopreservation and successful intra- and
Ž .
interspecies embryo transfer. J. Reprod. Fertil. 47, 189–201, Suppl. .
Pope, C.E., McRae, M.A., Plair, B.L., Keller, G.L., Dresser, D.L., 1994. Successful in vitro and in vivo development of in vitro fertilized two-to four-cell cat embryos following cryopreservation, culture and transfer. Theriogenology 42, 513–525.
Pope, C.E., Johnson, C.A., McRae, M.A., Keller, G.L., Dresser, B.L., 1995. In vitro development of domestic cat oocytes following intralytoplasmatic sperm injection and subzonal insemination. Therigenology 43,
Ž .
3602, abstr. .
Pope, C.E., McRae, M.A., Plair, B.L., Keller, G.L., Dresser, B.L., 1997. In vitro and in vivo development of embryos produced by in vitro maturation and in vitro fertilization of cat oocytes. J. Reprod. Fertil. 51, 69–82, Suppl.
Pope, C.E., Johnson, C.A., McRae, M.A., Keller, G.L., Dresser, B.L., 1998. Development of embryos produced by intracytoplasmatic sperm injection of cat oocytes. Anim. Reprod. Sci. 53, 221–236. Pope, C.E., Schmid, R., Dresser, D.L., 1999. In vitro development of cat embryos produced by in vitro
fertilization is enhanced by addition of cysteine to the maturation medium and a reduced O atmosphere.2
Ž .
Theriogenology 51, 291, abstr. .
Renton, J.P., Boyd, J.S., Eckersall, P.D., Ferguson, J.M., Harvey, M.J.A., Mullaney, J., Perry, B., 1991.
Ž .
Ovulation, fertilization and early embryonic development in the bitch Canis familiaris . J. Reprod. Fertil. 93, 221–231.
Robertson, J.B., Srsen, V., King, W.A., 1992. Cytogenetic and ultrastructural analysis of canine oocytes cultured in vitro. Proc. 12th Int. Congr. Anim. Reprod. 4, 1808–1810.
Rota, A., 1998. Studies on preservation, capacitation and fertility of dog spermatozoa. Thesis, Swedish Agricultural University, Uppsala, Sweden, 127 pp.
Rota, A., Strom, B., Linde-Forsberg, C., Rodriguez-Martinez, H., 1997. Effects of Equex STM paste on¨
viability of frozen thawed dog spermatozoa during in vitro incubation at 388C. Theriogenology 47, 1093–1101.
Rota, A., Iguer-Ouada, M., Verstegen, J., Linde-Forsberg, C., 1999. Fertility after vaginal or uterine deposition of dog semen frozen in a TRIS extender with or without Equex STM paste. Theriogenology 51, 1045–1058.
Roth, T.L., Swanson, W.F., Wildt, D.E., 1994. Developmental competence of domestic cat embryos fertilized in vivo versus in vitro. Biol. Reprod. 51, 441–451.
Schramm, R.D., Bavister, B., 1995. Effects of gonadotrophins, growth hormone and prolactin on developmen-tal competence of domestic cat oocytes matured in vitro. Reprod. Fertil. Dev. 7, 1061–1066.
Sparks, A.E.T., Gwazdauskas, F.C., McGilliard, M.L., 1992. Culture of one-cell bovine embryos in explanted mouse oviduct and bovine oviductal epithelial cells. Theriogenology 37, 587–594.
Spindler, R.E., Wildt, D.E., 1999. Relationship of substrate metabolism to cat oocyte maturation.
Theriogenol-Ž .
ogy 51, 295, abstr. .
Srsen, V., Kalous, J., Nagyova, E., Sutovsky, P., King, W.A., Motlik, J., 1998. Effects of follicle stimulating hormone, bovine somatotrophin and okadaic acid on cumulus expansion and nuclear maturation of blue fox
ŽAlopex lagopus oocytes in vitro. Zygote 6, 299–309..
Strom Holst, B., 1999. In vitro characterization of cryopreserved canine spermatozoa. Thesis, Swedish¨
University of Agricultural Sciences, Uppsala, Sweden, 90 pp.
Swanson, W.F., Howard, J.G., Roth, T.L., Brown, J.L., Alvarado, T., Burton, M., Starnes, D., Wildt, D.E., 1996a. Responsiveness to exogenous gonadotrophins and laparoscopic artificial insemination with frozen
Ž .
thawed spermatozoa in ocelots Felis pardalis . J. Reprod. Fertil. 106, 87–94.
Swanson, W.F., Roth, T.L., Godke, R.A., 1996b. Persistence of the developmental block to temporal variations in culture conditions. Mol. Reprod. Dev. 43, 298–305.
Swanson, W.F., Penfold, L.M., Wildt, D.E., 1998. Developmental capacity of IVF-derived domestic cat
Ž .
embryos following transfer to naturally-estrual, GnRH treated recipients. Theriogenology 49, 267, abstr. . Swanson, W.F., McRae, M.A., Wildt, D.E., Rall, W.F., 1999. Cryoprotectant toxicity and cryopreservation
Ž .
success in IVF derived domestic cat embryos after embryo transfer. Theriogenology 51, 174, abstr. . Szasz, F., Cheng, F.P., Marks, A., Colenbrander, B., Solti, L., 1997. Induction of the acrosome reaction in dog
sperm by calcium ionophore. Acta Vet. Hung. 45, 177–187.
Theiss, T., 1997. Investigations on the collection, in vitro maturation and-fertilization of dog oocytes. Thesis, Tierartzliche Fakultat der Ludwig-Maximillian Universitat Munich, 97 pp.¨ ¨
Tsutsui, T., Shimada, K., Nishi, M., Kubo, N., Murao, I., Shimizu, T., Ogasa, A., 1989. An experimental trial on embryo transfer in the dog. Jpn. J. Vet. Sci. 51, 797–800.
Ž
Wen, X.H., Feng, H.L., Sun, Q.Y., 1994. In vitro maturation of follicular oocytes of the silver fox Vulpes
. Ž .
fulÕa desm . Theriogenology 41, 333, abstr. .
Wildt, D.E., Monfort, S.L., Donoghue, A.M., Johnston, L.A., Howard, J., 1992. Embryogenesis in conserva-tion biology — or, how to make an endangered species embryo. Theriogenology 37, 161–184.
Wolfe, B.A., Wildt, D.E., 1996. Development to blastocysts from in vitro maturation and fertilization of domestic cat oocytes following prolonged cold storage ex situ. J. Reprod. Fertil. 106, 135–141. Wood, T.C., Wildt, D.E., 1997. Effect of the quality of cumulus-oocyte complex in the domestic cat on the
ability of oocytes to mature, fertilize and develop into blastocysts in vitro. J. Reprod. Fertil. 110, 355–360. Wood, T.C., Swanson, W.F., Davis, R.M., Anderson, J.E., Wildt, D.E., 1993. Functionality of sperm from normo- versus teratospermic domestic cats cryopreserved in pellets or straw containers. Theriogenology
Ž .
39, 342, abstr. .
Wood, T.C., Byers, A.P., Jennette, B.E., Wildt, D.E., 1995. Influence of protein and hormone supplementation on in vitro maturation and fertilization of domestic cat eggs. J. Reprod. Fertil. 104, 315–323.
Wood, T.C., Montali, R.J., Wildt, D.E., 1997. Follicle oocyte atresia and temporal taphonomy in cold stored domestic cat ovaries. Mol. Reprod. Dev. 46, 190–200.
Yamada, S., Shimazu, Y., Kawaji, H., Nakazawa, M., Naito, K., Toyoda, Y., 1992. Maturation, fertilization and development of dog oocytes in vitro. Biol. Reprod. 46, 853–858.
Yamada, S., Shimazu, Y., Kawao, Y., Nakazawa, M., Naito, K., Toyoda, Y., 1993. In vitro maturation and
Ž .
