Factors affecting in vitro embryo production: insights into dromedary camel

다국어 초록 (Multilingual Abstract)

The Dromedary camel (Camelus dromedaries) is an important species because of its ability to produce good quality meat, milk, and fibers under harsh environmental conditions. Camels are also crucial for transportation, racing, and as draft animals in agriculture. Therefore, dromedary camels play a critical role in the economy for millions of people living in the arid part of the world. The inherent capability of camels to produce meat and milk is highly correlated with their reproductive performance. Compared with other domestic species, the reproductive efficiency in camelids is low. Although recent reproductive technologies such as in vitro fertilization (IVF) and somatic cell nuclear transfer (SCNT) have been successfully applied to camelids and the birth of live offspring following these technologies has been reported; in vitro embryo production (IVP) has lagged in this species. The development of the IVP system for dromedary camels may be a useful tool for the genetic improvement of this species. IVP in farm animals includes three main steps; in vitro maturation (IVM) of an oocyte, IVF of a matured oocyte, and in vitro culture (IVC) of fertilized oocyte up to the blastocyst stage. This review aims to summarize various factors that influence oocyte quality, IVM, and in vitro embryo development in dromedary camel.

참고문헌 (Reference)

• 1 Moawad AR, "l-carnitine supplementation during vitrification of mouse germinal vesicle stage-oocytes and their subsequent in vitro maturation improves meiotic spindle configuration and mitochondrial distribution in metaphase II oocytes" 29 : 2256-2268, 2014
• 2 Tibary A, "Update on reproductive biotechnologies in small ruminants and camelids" 64 : 618-638, 2005
• 3 Wani NA, "Ultrasonographic-guided retrieval of cumulus oocyte complexes after super-stimulation in dromedary camel (Camelus dromedarius)" 74 : 436-442, 2010
• 4 Choi I, "Treatment of ovine oocytes with caffeine increases the accessibility of DNase I to the donor chromatin and reduces apoptosis in somatic cell nuclear transfer embryos" 22 : 1000-1014, 2010
• 5 Brogliatti GM, "Transvaginal collection and ultrastructure of llama(Lama glama)oocytes" 54 : 1269-1279, 2000
• 6 Madan ML, "Third World Buffalo Congress, Bulgaria, Varna, May 1991: Post-Congress Proceedings Volume" Agricultural Academy 11-17, 1991
• 7 Tibary A, "Theriogenology in camelidae:anatomy, physiology, pathology and artificial breeding" Actes Editions 1997
• 8 Stroud B, "The year 2011 worldwide statistics of embryo transfer in domestic farm animals" 50 : 16-25, 2012
• 9 Yanagimachi R, "The use of zona-free animal ova as a test-system for the assessment of the fertilizing capacity of human spermatozoa" 15 : 471-476, 1976
• 10 Ikeda S, "The roles of vitamin A for cytoplasmic maturation of bovine oocytes" 51 : 23-35, 2005
• 11 Skidmore JA, "The ovarian follicular wave pattern in the mated and non-mated dromedary camel(Camelus dromedarius)" 49 : 545-548, 1995
• 12 Musa BE, "The oestrous cycle of the camel (Camelus dromedarius)" 103 : 556-557, 1978
• 13 Liang S, "The influence of 9-cis-retinoic acid on nuclear and cytoplasmic maturation and gene expression in canine oocytes during in vitro maturation" 77 : 1198-1205, 2012
• 14 Khatir H, "The first dromedary (Camelus dromedarius) offspring obtained from in vitro matured, in vitro fertilized and in vitro cultured abattoir-derived oocytes" 65 : 1727-1736, 2006
• 15 Grupen CG, "The evolution of porcine embryo in vitro production" 81 : 24-37, 2014
• 16 Rieger D, "The effects of epidermal growth factor and insulin-like growth factor I on the metabolic activity, nuclear maturation and subsequent development of cattle oocytes in vitro" 112 : 123-130, 1998
• 17 Nasiri E, "The effect of retinoic acid on in vitro maturation and fertilization rate of mouse germinal vesicle stage oocytes" 13 : 19-24, 2011
• 18 Lonergan P, "The effect of recovery method on the type of bovine oocyte obtained for in vitro maturation" 35 : 231-, 1991
• 19 Daen FP, "The effect of pig follicular fluid fractions on cumulus expansion and male pronucleus formation in porcine oocytes matured and fertilized in vitro" 101 : 667-673, 1994
• 20 Moodie G, "The effect of incubating sheep ovaries for various times and temperatures on oocyte maturation rates in vitro" 40 : 53-, 1989
• 21 Nowshari MA, "The effect of harvesting technique on efficiency of oocyte collection and different maturation media on the nuclear maturation of oocytes in camels (Camelus dromedarius)" 63 : 2471-2481, 2005
• 22 Tellado MN, "The conditions of ovary storage affect the quality of porcine oocytes" 2 : 57-67, 2014
• 23 Pincus G, "The comparative behavior of mammalian eggs in vivo and in vitro: i. The activation of ovarian eggs" 62 : 665-675, 1935
• 24 Del Campo MR, "The application of new reproductive technologies to South American camelids" 43 : 21-30, 1995
• 25 Chen BX, "The Camelid: An All-Purpose Animal, 1" Scandinavian Institute of African Studies 364-386, 1979
• 26 Wilson RT, "The Camel" Longman 83-102, 1984
• 27 Lonergan P, "The ART of studying early embryo development : progress and challenges in ruminant embryo culture" 81 : 49-55, 2014
• 28 Atikuzzaman M, "The 9-cis retinoic acid signaling pathway and its regulation of prostaglandin-endoperoxide synthase 2 during in vitro maturation of pig cumulus cell-oocyte complexes and effects on parthenogenetic embryo production" 84 : 1272-1281, 2011
• 29 Niwa K, "Synergistic effect of caffeine and heparin on in-vitro fertilization of cattle oocytes matured in culture" 30 : 733-741, 1988
• 30 Takahashi T, "Supplementation of culture medium with L-carnitine improves development and cryotolerance of bovine embryos produced in vitro" 25 : 589-599, 2013
• 31 Akaki Y, "Successful piglet production in a chemically defined system for in-vitro production of porcine embryos : dibutyryl cyclic amp and epidermal growth factor-family peptides support in-vitro maturation of oocytes in the absence of gonadotropins" 55 : 446-453, 2009
• 32 Schernthaner W, "Storing bovine ovaries for 24 hours between 15 and 21°C does not influence in vitro production of blastocysts" 47 : 297-, 1997
• 33 Garbers DL, "Stimulation and maintenance of ejaculated bovine spermatozoan respiration and motility by caffeine" 5 : 336-339, 1971
• 34 Downs SM, "Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro" 41 : 371-379, 1989
• 35 Shalash MR, "Some reproductive aspects in the female camel" 1 : 103-108, 1965
• 36 Xia GL, "Short time priming of pig cumulus-oocyte complexes with FSH and forskolin in the presence of hypoxanthine stimulates cumulus cells to secrete a meiosis-activating substance" 53 : 1807-1815, 2000
• 37 Solano R, "Short term preservation of intrafollicular oocytes at 4°C" 41 : 299-, 1994
• 38 Downs SM, "Serum maintains the fertilizability of mouse oocytes matured in vitro by preventing hardening of the zona pellucida" 15 : 115-122, 1986
• 39 Sghiri A, "Seasonal effects on fertility and ovarian follicular growth and maturation in camels (Camelus dromedarius)" 55 : 223-237, 1999
• 40 Visconti PE, "Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm" 61 : 76-84, 1999
• 41 Marteil G, "Role of oocyte quality in meiotic maturation and embryonic development" 9 : 203-224, 2009
• 42 Morriss-Kay GM, "Retinoids and mammalian development" 188 : 73-131, 1999
• 43 Tsafriri A, "Resumption of oocyte meiosis in mammals : on models, meiosis activating sterols, steroids and EGF-like factors" 234 : 37-45, 2005
• 44 Skidmore JA, "Reproductive physiology in female Old World Camelids" 124 : 148-154, 2011
• 45 El-Wishy AB, "Reproduction in the female dromedary (Camelus dromedarius): a review" 15 : 273-297, 1987
• 46 Novoa C, "Reproduction in Camelidae" 22 : 3-20, 1970
• 47 Arthur GH, "Reproduction and genital diseases of the camel" 141 : 650-659, 1985
• 48 Bevers MM, "Regulation and modulation of oocyte maturation in the bovine" 47 : 13-22, 1997
• 49 Paramio MT, "Recent advances in in vitro embryo production in small ruminants" 86 : 152-159, 2016
• 50 Dunning KR, "Promoting lipid utilization with l-carnitine to improve oocyte quality" 134 : 69-75, 2012
• 51 Trasorras VL, "Production, preservation, and transfer of South American Camelid embryos" 4 : 190-, 2017
• 52 Wani NA, "Production of the first cloned camel by somatic cell nuclear transfer" 82 : 373-379, 2010
• 53 Sansinena MJ, "Production of nuclear transfer llama (lama glama)embryos from in vitro matured llama oocytes" 5 : 191-198, 2003
• 54 Khatir H, "Production of dromedary (Camelus dromedarius) embryos by IVM and IVF and coculture with oviductal or granulosa cells" 62 : 1175-1185, 2004
• 55 Fathi M, "Production of blastocysts following in vitro maturation and fertilization of dromedary camel oocytes vitrified at the germinal vesicle stage" 13 : e0194602-, 2018
• 56 Konishi M, "Presence of granulosa cells during oocyte maturation improved in vitro development of IVM-IVF bovine oocytes that were collected by ultrasound-guided transvaginal aspiration" 45 : 573-581, 1996
• 57 Bou SG, "Preliminary study on in vitro fertilization in the domestic camel (Camelus bactrianus)" 28 : 35-37, 1993
• 58 Lu KH, "Pregnancy established in cattle by transfer of embryos derived from in vitro fertilisation of oocytes matured in vitro" 121 : 259-260, 1987
• 59 Galli C, "Practical aspects of IVM/IVF in cattle" 42 : 371-379, 1996
• 60 Shimada M, "Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor" 20 : 1352-1365, 2006
• 61 Yasin SA, "Pakistan camels. A preliminary survey" 8 : 289-297, 1957
• 62 Kan M, "Oxygen-dependent growth declining and effect of vitamin E for human diploid fibroblasts in serum-free, BSA-containing culture" 139 : 389-398, 1983
• 63 Moawad AR, "Ovine oocytes vitrified at germinal vesicle stage as cytoplast recipients for somatic cell nuclear transfer (SCNT)" 13 : 289-296, 2011
• 64 Yaqoob SH, "Optimizing camel (Camelus dromedarius) oocytes in vitro maturation and early embryo culture after parthenogenetic activation" 153 : 81-86, 2017
• 65 Kumar A, "Oocyte retrieval and histological studies of follicular population in buffalo ovaries" 47 : 189-195, 1997
• 66 Tinson AH, "Oocyte collection techniques in the dromedary camel" 13 : 39-45, 2001
• 67 Austin CR, "Observations on the penetration of the sperm in the mammalian egg" 4 : 581-596, 1951
• 68 El-Wishy AB, "Observations on the ovaries of slaughtered camels (Camelus dromedarius)" 32 : 295-312, 1984
• 69 Tamilmani G, "Nuclear maturation of ovine oocytes in cultured preantral follicles" 60 : 295-305, 2005
• 70 Brackett BG, "Normal development following in vitro fertilization in the cow" 27 : 147-158, 1982
• 71 Abdoon AS, "Morphology of dromedary camel oocytes and their ability to spontaneous and chemical parthenogenetic activation" 42 : 88-93, 2007
• 72 Richani D, "Mode of oocyte maturation affects EGF-like peptide function and oocyte competence" 19 : 500-509, 2013
• 73 Dale B, "Mechanism of fertilization" 325 : 762-763, 1987
• 74 Kikuchi K, "Maturation/M-phase promoting factor : a regulator of aging in porcine oocytes" 63 : 715-722, 2000
• 75 Lonergan P, "Maturation of oocytes in vitro" 4 : 255-268, 2016
• 76 Edwards RG, "Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes" 208 : 349-351, 1965
• 77 Ball GD, "Maturation and fertilization of bovine oocytes in vitro" 67 : 2775-2785, 1984
• 78 Marie M, "Mating-induced luteinizing hormone surge and ovulation in the female camel (Camelus dromedarius)" 35 : 792-798, 1986
• 79 Zuelke KA, "Luteinizing hormoneenhanced in vitro maturation of bovine oocytes with and without protein supplementation" 43 : 784-787, 1990
• 80 Nili H, "Light and transmission electron microscopy of immature camelus dromedarius oocyte" 33 : 196-199, 2004
• 81 Mansour G, "L-carnitine supplementation reduces oocyte cytoskeleton damage and embryo apoptosis induced by incubation in peritoneal fluid from patients with endometriosis" 91 (91): 2079-2086, 2009
• 82 Moawad AR, "L-carnitine supplementation during vitrification of mouse oocytes at the germinal vesicle stage improves preimplantation development following maturation and fertilization in vitro" 88 : 104-, 2013
• 83 Fathi M, "L-carnitine enhances oocyte maturation and improves in vitro development of embryos in dromedary camels (Camelus dromedaries)" 104 : 18-22, 2017
• 84 Abdelrazik H, "L-carnitine decreases DNA damage and improves the in vitro blastocyst development rate in mouse embryos" 91 : 589-596, 2009
• 85 Wani NA, "Kinetics of nuclear maturation and effect of holding ovaries at room temperature on in vitro maturation of camel (Camelus dromedarius) oocytes" 64 : 75-85, 2005
• 86 Skidmore JA, "Investigation of factors affecting pregnancy rate after embryo transfer in the dromedary camel" 14 : 109-116, 2002
• 87 Glogowski J, "Inhibition of alkaline phosphatase activity of boar semen by pentoxifylline, caffeine, and theophylline" 23 : 783-792, 2002
• 88 Martino A, "Influence of the collection technique of prepubertal goat oocytes on in vitro maturation and fertilization" 42 : 859-873, 1994
• 89 Younis AI, "Influence of serum and hormones on bovine oocyte maturation and fertilization in vitro" 23 : 189-201, 1989
• 90 Sutton ML, "Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes" 126 : 27-34, 2003
• 91 Abdoon AS, "Influence of oocyte quality, culture media and gonadotropins on cleavage rate and development of in vitro fertilized buffalo embryos" 65 : 215-223, 2001
• 92 Lorenzo PL, "Influence of epidermal growth factor on mammalian oocyte maturation via tyrosine-kinase pathway" 57 : 15-22, 2001
• 93 Downs SM, "Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor : evidence for a positive stimulus of somatic cell origin" 245 : 86-96, 1988
• 94 Goud PT, "In-vitro maturation of human germinal vesicle stage oocytes : role of cumulus cells and epidermal growth factor in the culture medium" 13 : 1638-1644, 1998
• 95 Sansinena MJ, "In vitro production of llama (Lama glama) embryos by intracytoplasmic sperm injection: effect of chemical activation treatments and culture conditions" 99 : 342-353, 2007
• 96 Abdelkhalek AE, "In vitro production of Sudanese camel(Camelus dromedarius)embryos from epididymal spermatozoa and follicular oocytes of slaughtered animals" 20 : 95-101, 2017
• 97 Totey SM, "In vitro maturation, fertilization and development of follicular oocytes from buffalo (Bubalus bubalis)" 95 : 597-607, 1992
• 98 Eckert J, "In vitro maturation, fertilization and culture to blastocysts of bovine oocytes in protein-free media" 43 : 1211-1125, 1995
• 99 Del Campo MR, "In vitro maturation of llama (Lama glama) oocytes" 324-326, 1992
• 100 Ben-Ami I, "In vitro maturation of human germinal vesicle-stage oocytes : role of epidermal growth factor-like growth factors in the culture medium" 26 : 76-81, 2011
• 101 Wani N, "In vitro maturation of dromedary (Camelus dromedarius) oocytes: effect of different protein supplementations and epidermal growth factor" 45 : e189-e193, 2010
• 102 Ghoneim IM, "In vitro maturation of cumulus oocyte complexes of pregnant and non-pregnant Camelus dromedarius" 59 : 1649-1659, 1999
• 103 Zeidan AEB, "In vitro maturation of camel oocytes as affected by different media during breeding and non-breeding seasons" 7 : 460-472, 2011
• 104 Johnston LA, "In vitro maturation and fertilization of domestic cat follicular oocytes" 24 : 343-356, 1989
• 105 Moawad AR, "In vitro maturation and fertilization of camel oocytes" Cairo University 2005
• 106 Ravindranatha BM, "In vitro maturation and fertilization of buffalo oocytes : effects of storage of ovaries, IVM temperatures, storage of processed sperm and fertilization media" 38 : 21-26, 2003
• 107 Totey SM, "In vitro maturation and fertilization of buffalo oocytes (Bubalus bubalis): effects of media, hormones and sera" 39 : 1153-1171, 1993
• 108 Lenz RW, "In vitro maturation and fertilization of bovine oocytes are temperature-dependent processes" 29 : 173-179, 1983
• 109 Kafi M, "In vitro maturation and fertilization of bovine oocytes and in vitro culture of presumptive zygotes in the presence of bovine pestivirus" 71 : 169-179, 2002
• 110 Sreenan J, "In vitro maturation and attempted fertilization of cattle follicular oocytes" 75 : 393-396, 1970
• 111 Hanada A, "In vitro fetilization in goats" 31 : 21-26, 1985
• 112 Rath D, "In vitro fertilization of porcine oocytes with fresh and frozen-thawed ejaculated or frozenthawed epididymal semen obtained from identical boars" 47 : 785-793, 1997
• 113 Cheng WTK, "In vitro fertilization of pig and sheep oocytes matured in vivo and in vitro" 25 : 146-, 1986
• 114 Moawad AR, "In vitro fertilization of ovine oocytes vitrified by solid surface vitrification at germinal vesicle stage" 65 : 139-144, 2012
• 115 Del Campo MR, "In vitro fertilization of llama (Lama glama) follicular oocytes" 41 : 187-, 1994
• 116 Xu X, "In vitro fertilization of in vitro matured pig oocytes : effects of boar and ejaculate fraction" 45 : 745-755, 1996
• 117 Moawad AR, "In vitro fertilization of dromedary camel (Camelus dromedarius)oocytes with epididymal spermatozoa" 24 : 192-193, 2012
• 118 Palmer E, "In vitro fertilization in the horse. A retrospective study" 44 : 375-384, 1991
• 119 Del Campo MR, "In vitro fertilization and development of llama (Lama glama) oocytes using epididymal spermatozoa and oviductal cell co-culture" 41 : 1219-1229, 1994
• 120 Goto K, "In vitro fertilization and development of in vitro matured bovine follicular oocytes" 67 : 2181-2185, 1989
• 121 Berland MA, "In vitro fertilization and development of cumulus oocytes complexes collected by ultrasound-guided follicle aspiration in superstimulated llamas" 75 : 1482-1488, 2011
• 122 Yang NS, "In vitro fertilization (IVF) and culture (IVC) of bovine oocytes from stored ovaries" 33 : 352-, 1990
• 123 Wani NA, "In vitro embryo production in camel (Camelus dromedarius) from in vitro matured oocytes fertilized with epididymal spermatozoa stored at 4 degrees C" 111 : 69-79, 2009
• 124 Thompson JG, "In vitro culture and embryo metabolism of cattle and sheep embryos - a decade of achievement" 60-61 : 263-275, 2000
• 125 Samper JC, "In vitro capacitation of stallion spermatozoa in calciumfree Tyrode’s medium and penetration of zona-free hamster eggs" 31 : 875-884, 1989
• 126 Khatir H, "In vitro and in vivo developmental competence of dromedary (Camelus dromedarius) oocytes following in vitro fertilization or parthenogenetic activation" 113 : 212-219, 2009
• 127 Khatir H, "In vitro and in vivo developmental competence of dromedary (Camelus dromedarius) embryos produced in vitro using two culture systems (mKSOMaa and oviductal cells)" 40 : 245-249, 2005
• 128 Motlík J, "Impact of two‐step in vitro culture systems on developmental potency of oocytes" 35 : 267-271, 2000
• 129 O’Brien JK, "Hormonal requirements for in vitro maturation of sheep oocyte" 41 : 266-, 1994
• 130 Moor RM, "Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and their subsequent developmental capacity" 49 : 101-109, 1977
• 131 de Loos F, "Heterologous cell contacts and metabolic coupling in bovine cumulus oocyte complexes" 28 : 255-259, 1991
• 132 Kito S, "Gonadotropins, serum, and amino acids alter nuclear maturation, cumulus expansion, and oocyte morphology in hamster cumulus-oocyte complexes in vitro" 56 : 1281-1289, 1997
• 133 Eppig JJ, "Gonadotropin stimulation of the expansion of cumulus oophori isolated from mice : general conditions for expansion in vitro" 208 : 111-120, 1979
• 134 Livingston T, "Glutathione content and antioxidant enzyme expression of in vivo matured sheep oocytes" 116 : 265-273, 2009
• 135 El-Wishy AB, "Functional changes in the pregnant camel with special reference to foetal growth" 137 : 527-537, 1981
• 136 van den Hurk R, "Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles" 63 : 1717-1751, 2005
• 137 Schroeder AC, "Fetuin inhibits zona pellucida hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum" 43 : 891-897, 1990
• 138 Chang MC, "Fertilizing capacity of spermatozoa deposited into the fallopian tubes" 168 : 697-698, 1951
• 139 Chang MC, "Fertilization of rabbit ova in vitro" 184 (184): 466-467, 1959
• 140 Whittingham DG, "Fertilization of mouse eggs in vitro" 220 : 592-593, 1968
• 141 Iritani A, "Fertilization in vitro of cattle follicular oocytes with ejaculated spermatozoa capacitated in a chemically defined medium" 70 : 487-492, 1984
• 142 Abd El-Aziz AH, "Factors influencing in vitro production of bovine embryos : a review" 11 : 737-756, 2016
• 143 Ball GD, "Factors affecting successful in vitro fertilization of bovine follicular oocytes" 28 : 717-725, 1983
• 144 Abdoon AS, "Factors affecting follicular population, oocyte yield and quality in camels (Camelus dromedarius) ovary with special reference to maturation time in vitro" 66 : 71-79, 2001
• 145 Abdel-Rahim SEA, "Factors affecting camel reproductive performance in the tropics" Institut d’Elevage et de Medecine Veterinaire des Pays Tropicaux Etudes et Syntheses 131-148, 1993
• 146 Eppig JJ, "FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles" 281 : 483-484, 1979
• 147 Kitiyanant Y, "Evaluation of the acrosome reaction and viability in buffalo spermatozoa using two staining methods : the effects of heparin and calcium ionophore A23187" 25 : 215-222, 2002
• 148 Dekel N, "Epidermal growth factor induces maturation of rat follicle-enclosed oocytes" 116 : 406-409, 1985
• 149 Das K, "Epidermal growth factor in human follicular fluid stimulates mouse oocyte maturation in vitro" 57 : 895-901, 1992
• 150 Somfai T, "Enhancement of lipid metabolism with L-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes" 23 : 912-920, 2011
• 151 Skidmore JA, "Embryo transfer in the dromedary camel (Camelus dromedarius) using non-ovulated and ovulated, asynchronous progesterone-treated recipients" 23 : 438-443, 2011
• 152 Tibary A, "Embryo transfer in camelids" 5 : 234-252, 2015
• 153 Purohit GN, "Efficiency of three methods of oocyte recovery in the dromedary camel (Camelus dromedarius)" 69 : 88-90, 1999
• 154 Kito S, "Effects of volume, culture media and type of culture dish on in vitro development of hamster 1-cell embryos" 47 : 541-548, 1997
• 155 Aoyagi Y, "Effects of two treatments on semen from different bulls on in vitro fertilization results of bovine oocytes" 30 : 973-985, 1988
• 156 Jaakma U, "Effects of sperm treatments on the in vitro development of bovine oocytes in semidefined and defined media" 48 : 711-720, 1997
• 157 Fukui Y, "Effects of sera, hormones and granulosa cells added to culture medium for in-vitro maturation, fertilization, cleavage and development of bovine oocytes" 86 : 501-506, 1989
• 158 Wongsrikeao P, "Effects of ovary storage time and temperature on DNA fragmentation and development of porcine oocytes" 51 : 87-97, 2005
• 159 Kawakami E, "Effects of medium containing heparin and theophylline on capacitation and metabolic enzyme activities of ejaculated spermatozoa from dogs with asthenozoospermia" 54 : 251-259, 1999
• 160 Fukushima M, "Effects of gonadotropins and steroids on the subsequent fertilizability of extrafollicular bovine oocytes cultured in vitro" 9 : 323-332, 1985
• 161 Lee JH, "Effects of enucleation and caffeine on maturation-promoting factor (MPF) and mitogenactivated protein kinase (MAPK) activities in ovine oocytes used as recipient cytoplasts for nuclear transfer" 74 : 691-698, 2006
• 162 Yuge M, "Effects of cooling ovaries before oocyte aspiration on meiotic competence of porcine oocytes and of exposing in vitro matured oocytes to ambient temperature on in vitro fertilization and development of the oocytes" 47 : 102-108, 2003
• 163 Maalouf WE, "Effects of caffeine, cumulus cell removal and aging on polyspermy and embryo development on in vitro matured and fertilized ovine oocytes" 71 : 1083-1092, 2009
• 164 Saadeldin IM, "Effects of all-trans retinoic acid on the in vitro maturation of camel (Camelus dromedarius) cumulus-oocyte complexes" 65 : 215-221, 2019
• 165 Guignot F, "Effect of time during transport of excised mare ovaries on oocyte recovery rate and quality after in vitro maturation" 52 : 757-766, 1999
• 166 Shioya Y, "Effect of the time between slaughter and aspiration of follicles on the developmental capability of bovine oocytes matured and fertilized in vitro" 34 : 39-44, 1988
• 167 Datta TK, "Effect of quality of buffalo oocytes on their maturation rate in vitro" 69 : 23-26, 1999
• 168 Love LB, "Effect of ovary storage and oocyte transport method on maturation rate of horse oocytes" 59 : 765-774, 2003
• 169 Abdel-Khalek EA, "Effect of ovary preservation period on recovery rate and categories of dromedary camel oocytes" 17 : 231-235, 2010
• 170 Ratto M, "Effect of ovarian superstimulation on COC collection and maturation in alpacas" 97 : 246-256, 2007
• 171 Rose TA, "Effect of oocyte maturation medium on in vitro development of in vitro fertilized bovine embryos" 31 : 72-77, 1992
• 172 Procházka R, "Effect of epidermal growth factor-like peptides on pig cumulus cell expansion, oocyte maturation, and acquisition of developmental competence in vitro : comparison with gonadotropins" 141 : 425-435, 2011
• 173 Trasorras VL, "Effect of eCG superstimulation and buserelin on cumulus-oocyte complexes recovery and maturation in llamas (Lama glama)" 44 : 359-364, 2009
• 174 Nagai T, "Effect of cysteamine and FSH on in vitro maturation of porcine oocytes" 53 : 461-, 2000
• 175 Hemeida NA, "Effect of culture media and epidermal growth factor on in vitro oocyte maturation in the one-humped camel (Camelus dromedarius)" 8 : 130-141, 2015
• 176 Pandey A, "Effect of FSH and LH hormones on oocyte maturation of buffalo and gene expression analysis of their receptors and Cx43 in maturing oocytes" 18 : 231-234, 2010
• 177 Niwa K, "Early events of invitro fertilization of cat eggs by epididymal spermatozoa" 74 : 657-660, 1985
• 178 Scholkamy TH, "Developmental competence of Dromedary camel oocytes fertilized in vitro by frozen-thawed ejaculated and epididymal spermatozoa" 17 : 253-258, 2016
• 179 Bavister BD, "Development of in vitro matured/in vitro fertilized bovine embryos into morulae and blastocysts in defined culture media" 37 : 127-146, 1992
• 180 Tibary A, "Current knowledge and future challenges in camelid reproduction" 64 : 297-313, 2007
• 181 Bedford JM, "Cumulus oophorus as a sperm sequestering device, in vivo" 265 : 321-328, 1993
• 182 Bavister BD, "Culture of preimplantation embryos : facts and artifacts" 1 : 91-148, 1995
• 183 Smythe C, "Coupling of mitosis to the completion of S phase in Xenopus occurs via modulation of the tyrosine kinase that phosphorylates p34cdc2" 68 : 787-797, 1992
• 184 Lee CN, "Concentrations and composition of glycosaminoglycans in the female bovine reproductive tract" 67 : 2006-2009, 1984
• 185 Ravindranatha BM, "Comparison of three different media on maturation of buffalo oocytes in vitro" 71 : 841-843, 2001
• 186 Jain GC, "Comparative efficiency of three different collection techniques for oocyte retrieval in buffaloes" 43 : 240-, 1995
• 187 Kafi M, "Chronological and ultrastructural changes in camel(Camelus dromedarius)oocytes during in vitro maturation" 63 : 2458-2470, 2005
• 188 Mahmoud KG, "Chromosome configuration during in vitro maturation of dromedary camel oocytes" 51 : 411-420, 2003
• 189 Crichton EG, "Cholesterol addition aids the cryopreservation of dromedary camel (Camelus dromedarius) spermatozoa" 83 : 168-174, 2015
• 190 Steinmann KE, "Chemically induced premature mitosis : differential response in rodent and human cells and the relationship to cyclin B synthesis and p34cdc2/cyclin B complex formation" 88 : 6843-6847, 1991
• 191 Torner H, "Changes in cumulusoocyte complexes of pregnant and non-pregnant camels (Camelus dromedarius) during maturation in vitro" 60 : 977-987, 2003
• 192 Brackett BG, "Capacitation of rabbit spermatozoa in vitro" 12 : 260-274, 1975
• 193 Gadella BM, "Capacitation and the acrosome reaction in equine sperm" 68 : 249-265, 2001
• 194 Fathi M, "Caffeine supplementation during IVM improves frequencies of nuclear maturation and preimplantation development of dromedary camel oocytes following IVF" 81 : 1286-1292, 2014
• 195 Moawad AR, "Caffeine and oocyte vitrification: sheep as an animal model" 6 (6): S41-S48, 2018
• 196 El-Wishy AB, "Breeding activity of the camel (Camelus dromedarius)" 11 : 75-77, 1986
• 197 Yang X, "Bovine oocyte development following different oocyte maturation and sperm capacitation procedures" 34 : 94-100, 1993
• 198 Parrish JJ, "Bovine in vitro fertilization with frozen-thawed semen" 25 : 591-600, 1986
• 199 Parrish JJ, "Bovine in vitro fertilization : in vitro oocyte maturation and sperm capacitation with heparin" 81 : 67-73, 2014
• 200 Keefer CL, "Bovine embryo development in vitro : effect of in vitro maturation conditions on fertilization and blastocyst development" 35 : 223-, 1991
• 201 Yoshida M, "Birth of piglets derived from in vitro fertilization of pig oocytes matured in vitro" 39 : 1303-1311, 1993
• 202 Dunning KR, "Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development" 83 : 909-918, 2010
• 203 Yamada T, "Beneficial effects of acetylL-carnitine treatment during IVM on post-fertilization development of bovine oocytes in vitro" 18 : 280-281, 2006
• 204 Wright RW Jr, "Aspects of in vitro fertilization and embryo culture in domestic animals" 53 : 702-729, 1981
• 205 Brackett BG, "Analysis of factors involved in the in vitro production of bovine embryos" 39 : 43-64, 1993
• 206 Pu Y, "All-trans retinoic acid improves goat oocyte nuclear maturation and reduces apoptotic cumulus cells during in vitro maturation" 85 : 833-839, 2014
• 207 Köhler-Rollefson I, "About camel breeds : a reevaluation of current classification systems" 110 : 66-73, 1993
• 208 Chen J, "AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro" 313 : 47-57, 2008
• 209 Pawshe CH, "A comparison of three methods of recovery of goat oocytes for in vitro maturation and feritilization" 42 : 117-125, 1994