Abstract
Since the generation of buffalo embryonic stem cells (ESCs) from the inner cell mass (ICM) of blastocysts in 2004 to till date, significant progress has been achieved in this species. Derivation and maintenance of ESCs from blastocysts generated by parthenogenesis, in vitro fertilization and nuclear transfer showed a steady progress towards finding the optimal conditions for the derivation of stable and highly competent buffalo ESCs. The molecular mechanisms for self-renewal of buffalo ESCs and the role of various growth factors involved therein as well as differentiation capacity were explored to a great extent. Although some reports showed the successful isolation and long-term culture of buffalo ESCs in vitro, but many studies were not able to establish suitable conditions for preventing spontaneous differentiation and senescence of ESCs. Hence a need to search alternative ways of deriving unipotent, pluripotent or multipotent stem cells in buffaloes always remained in trend. Therefore, in the present review, we analyse the available data on buffalo ESCs to have a better understanding about the strengths and weaknesses of the buffalo ESC has been analysed generation, which could help in the production of validated ESC lines in this species, besides the recent progress in buffalo fetal and adult tissue derived stem cells, which could be established as an alternative source of ESCs.
Similar content being viewed by others
References
Adewumi O, Aflatoonia B, Ahrlund-Richte L, Amit M, Andrews PW, Beighton G, Bello PA (2007) Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25:803–816
Anand T, Kumar D, Singh MK, Shah RA, Chauhan MS, Manik RS, Singla SK, Palta P (2011) Buffalo (Bubalus bubalis) embryonic stem cell-like cells and preimplantation embryos exhibit comparable expression of pluripotency related antigens. Reprod Dom Anim 46:50–58
Anjana P, Kumanan K, Parthiban M, Balasubramaniam S (2012) Isolation and characterization of buffalo amniotic fluid stem cells. Indian J Anim Sci 82:577–580
Capecchi MR (1989) Altering the genome by homologous recombination. Science 244:1288–1292
Carpenter MK, Bhatia M (2004) In: Lanza Robert (ed) Characterization of human embryonic stem cells, handbook of stem cells, vol 1. Elsevier, Amsterdam, pp 407–411
Chantaraprateep P, Lohachit C, Techakumphu M, Kobayashi G, Virakul P, Kunayongkrit A, Prateep P, Limskul A (1989) Early embryonic development in Thai swamp buffalo (Bubalus bubalis). Theriogenology 31(6):1131–1139
Chauhan MS, Verma V, Manik RS, Palta P, Singla SK, Goswami SL (2005) Development of inner cell mass and formation of embryoid bodies on a gelatin-coated dish and on the feeder layer in buffalo (Bubalus bubalis). Reprod Fertil Dev 18:205–206
Chen LR, Shiue YL, Bertolini L, Medrano JF, BonDurant RH, Anderson GB (1999) Establishment of pluripotent cell lines from porcine preimplantation embryos. Theriogenology 52:195–212
Clark AT, Rodriguez RT, Bodnar MS, Abeyta MJ, Cedars MI, Turek PJ, Firpo MT, Pera RRA (2004) Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma. Stem Cells 22:169–179
Coli A, Nocchi F, Lamanna R, Iorio M, Lapi S, Urciuoli P, Scatena F, Giannessi E, Stornelli MR, Passeri S (2011) Isolation and characterization of equine amnion mesenchymal stem cells. Cell Biol Int Rep 18:23–29
Cremonesi F, Corradetti B, Lange CA (2011) Fetal adnexa derived stem cells from domestic animal: progress and perspectives. Theriogenology 75:1400–1415
Degrelle SA, Campion E, Cabau C, Piumi F, Reinaud P, Richard C, Renard JP, Hue E (2005) Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev Biol 288:448–460
Deng Y, Liu Q, Luo C, Chen S, Li X, Wang C, Liu Z, Lei X, Zhang H, Sun H, Lu F, Jiang J, Shi D (2012) Generation of induced pluripotent stem cells from buffalo (Bubalus bubalis) fetal fibroblasts with buffalo defined factors. Stem Cells Dev 21:2485–2494
Dev K, Gautam SK, Giri SK, Kumar A, Yadav A, Verma V, Kumar P, Singh B (2012) Isolation, culturing and characterization of feeder-independent amniotic fluid stem cells in buffalo (Bubalus bubalis). Res Vet Sci 93:743–748
Dev K, Giri SK, Kumar A, Yadav A, Singh B, Gautam SK (2012) Derivation, characterization and differentiation of buffalo (Bubalus bubalis) amniotic fluid derived stem cells. Reprod Dom Anim 47:704–711
Draper JS, Pigott C, Thomson JA, Andrews PW (2002) Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat 200:249–258
Drost M, Elsden RP (1985) Blastocyst development in water buffalo (Bubalus bubalis). Theriogenology 23:191
Dyce PW, Hai Z, Jesse C, Julang L (2004) Stem cells with multilineage potential derived from porcine skin. Biochem Biophys Res Commun 316:651–658
Eiselleova L, Peterkova I, Neradil J, Slaninova I, Hampl A, Dvorak P (2008) Comparative study of mouse and human feeder cells for human embryonic stem cells. Int J Dev Biol 52:353–363
Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotent cells from mouse embryo. Nature 292:154–156
Gade NE, Pratheesh MD, Nath A, Dubey PK, Sharma B, Saikumar G, Sharma GT (2013) Molecular and cellular characterization of buffalo bone marrow-derived mesenchymal stem cells. Reprod Dom Anim 48:358–367
Gasparrini B, Sayoud H, Neglia G, de Matos DG, Donnay I, Zicarelli L (2003) Glutathione synthesis during in vitro maturation of buffalo (Bubalus bubalis) oocytes: effects of cysteamine on embryo development. Theriogenology 60:943–952
George A, Sharma R, Singh KP, Panda KP, Singla SK, Palta P, Manik RS, Chauhan MS (2011) Production of cloned and transgenic embryos using buffalo (Bubalus bubalis) embryonic stem cell-like cells isolated from in vitro-fertilized and cloned blastocysts. Cell Reprogramming 13(3):263–272
Gjørret JO, Maddox-Hyttel P (2005) Attempts towards derivation and establishment of bovine embryonic stem cell-like cultures. Reprod Fertil Dev 17:113–124
Goel S, Reddy N, Mandal S, Kim S, Fujihara M, Kim SM, Imai H (2010) Spermatogonia specific proteins expressed in prepubertal buffalo (Bubalus bubalis) testis and their utilization for isolation and in vitro cultivation of spermatogonia. Theriogenology 74:1221–1232
Guest DJ, Allen WR (2007) Expression of cell surface antigens and embryonic stem cell pluripotency genes in equine blastocysts. Stem Cells Dev 16:789–795
Hatoya S, Torii R, Kondo Y, Okuno T, Kobayashi K, Wijewardana V, Kawate N, Tamada H, Sawada T, Kumagai D, Sugiura K, Inaba T (2006) Isolation and characterization of embryonic stem like cells from canine blastocysts. Mol Reprod Dev 73:298–305
Henderson JK, Draper JS, Baillie HS, Fishel S, Thomson JA, Moore H, Andrews PH (2002) Preimplantation human embryos and embryonic stem cells show comparable expression of stage-specific embryonic antigens. Stem Cells 20:329–333
Hepsibha P, Meenambigai TV, Mangalagowri A, Palanisamy A, Stalin A, Nithya S, Kumanan K (2011) Multipotent differentiation potential of buffalo adipose tissue derived mesenchymal stem cells. Asian J Anim Vet Adv 6:772–788
Honda A, Hirose M, Ogura A (2009) Basic FGF and activin/nodal but not LIF signaling sustain undifferentiated status of rabbit embryonic stem cells. Exp Cell Res 315:2033–2042
Huang B, Li T, Wang XL, Xie TS, Lu YQ, da Silva FM, Shi DS (2010) Generation and characterization of embryonic stem like cell lines derived from in vitro fertilization buffalo (Bubalus bubalis) embryos. Reprod Dom Anim 45:122–128
Huang B, Xie TS, Shi DS, Li T, Wang XL, Mo Y, Wang ZQ, Li MM (2007) Isolation and characterization of EG-like cells from Chinese swamp buffalo (Bubalus bubalis). Cell BiolInt 31:1079–1088
Humphrey RK, Beattie GM, Lopez AD, Bucay N, King CC, Firpo MT, Rose-John S, Hayek A (2004) Maintenance of pluripotency in human embryonic stem cells is STAT3 independent. Stem Cells 22:522–530
Jiang HS, Wang WL, Lu KH, Gordon I, Polge C (1992) Examination of cell numbers of blastocysts derived from IVM, IVF and IVC of bovine follicular oocytes. Theriogenology 37:229
Kala S, Kaushik R, Singh KP, Kadam PH, Singh MK, Manik RS, Singla SK, Palta P, Chauhan MS (2012) In vitro culture and morphological characterization of prepubertal buffalo (Bubalus bubalis) putative spermatogonial stem cell. J Assist Reprod Genet 29:1335–1342
Karaivanov C, Vlahov K, Petrov M, Kacheva D, Stojanova M, Alexiev A, Polihronov O, Danev A (1987) Studies on preimplantation development of buffalo embryos. Theriogenology 28(5):747–753
Keefer CL, Pant D, Blomberg L, Talbot NC (2007) Challenges and prospects for the establishment of embryonic stem cell lines of domestic ungulates. Anim Reprod Sci 98:147–168
Kitiyanant Y, Saikhun J, Kitiyanant N, Sritanaudomchai H, Faisaikarm T, Pavasuthipaisit K (2004) Establishment of buffalo embryonic stem-like (ES-like) cell lines from different sources of derived blastocysts. Reprod Fertil Dev 16:216
Kumar A, Kumar K, Singh R, Puri G, Ranjan R, Yasotha T, Singh RK, Sarkar M, Bag S (2012) Effect of mitotic inducers and retinoic acid blocker on expression of pluripotent genes in ES cells derived from early stage in vitro-produced embryos in buffalo. In Vitro Cell Dev Biol Anim 48:625–632
Kumar D, Anand T, Singh KP, Shah RA, Singh MK, Chauhan MS, Palta P, Singla SK, Manik RS (2012) Generation of buffalo embryonic stem cell-like cells from in vitro produced, day 8 hatched and day 9 expanded blastocysts. Indian J Anim Sci 82:838–843
Kumar D, Anand T, Singh KP, Singh MK, Shah RA, Chauhan MS, Singla SK, Palta P, Manik RS (2011) Derivation of buffalo embryonic stem-like cells from in vitro-produced blastocysts on homologous and heterologous feeder cells. J Assist Reprod Genet 28:679–688
Li M, Ma W, Hou Y, Sun XF, Sun QY, Wang WH (2004) Improved isolation and culture of embryonic stem cells from Chinese miniature pig. J Reprod Dev 50:237–244
Liang X, Zhang X, Yang B, Cheng M, Huang F, Pang C, Qing G, Liao C, Wei S, Senatore EM, Bella A, Presicce GA (2007) Pregnancy and calving rates following transfer of in vitro-produced river and F1 (river × swamp) buffalo (Bubalus bubalis) embryos in recipients on natural oestrus or synchronized for ovulation. Reprod Fertil Dev 19:670–676
Lonergan P, Fair T, Corcoran D, Evans AC (2006) Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology 65:137–152
Maddox-Hyttel P, Alexopoulos NI, Vajta G, Lewis I, Rogers P, Cann L, Callesen H, Tveden-Nyborg P, Trounson A (2003) Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125:607–623
Mahla RS, Reddy N, Goel S (2012) Spermatogonial stem cells (SSCs) in buffalo (Bubalus bubalis) testis. PLoS One 7:e36020
Mann A, Yadav RP, Singh J, Kumar D, Singh B, Yadav PS (2013) Culture, characterization and differentiation of cells from buffalo (Bubalus bubalis) amnion. Cytotechnology 65:23–30
Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 78:7634–7638
Miki T, Strom SC (2006) Amnion-derived pluripotent/multipotent stem cells. Stem Cell Rev 2:133–142
Mitalipova M, Beyhan Z, First NL (2001) Pluripotency of bovine embryonic cell line derived from precompacting embryos. Cloning 3:59–67
Monson R, Northey DL, Gottfredson R, Peschel DR, Rutledge JJ, Shaefer DM (1992) Pregnancy rates of in vitro produced bovine embryos following non-surgical transfer. Theriogenology 37:261
Munoz M, Dıez C, Caamano JN, Jouneau A, Hue I, Gomez E (2008) Embryonic stem cells in cattle. Reprod Dom Anim 43(Suppl 4):32–37
Munoz M, Rodriguez A, De Frutos C, Caamano JN, Dıez C, Facal N, Gomez E (2008) Conventional pluripotency markers are unspecific for bovine embryonic derived cell-lines. Theriogenology 69:1159–1164
Muzaffar M, Selokar NL, Singh KP, Zandi M, Singh MK, Shah RA, Chauhan MS, Singla SK, Palta P, Manik R (2012) Equivalency of buffalo (Bubalus bubalis) embryonic stem cells derived from fertilized, parthenogenetic and handmade cloned embryos. Cell Reprogramming 14:267–279
Nandi S, Raghu HM, Ravindranatha BM, Chauhan MS (2002) Production of buffalo (Bubalus bubalis) embryos in vitro: premises and promises. Reprod Domest Anim 37:65–74
Narula A, Taneja M, Totey SM (1996) Morphological development, cell number and allocation of cells to trophectoderm and inner cell mass of in vitro fertilized and parthenogenetically developed buffalo embryos: the effect of IGF–I. Mol Reprod Dev 44:343–351
Niwa H, Burdon T, Chambers I, Smith A (1998) Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 12:2048–2060
Palta P, Chauhan MS (1998) Laboratory production of buffalo (Bubalus bubalis) embryos. Reprod Fertil Dev 10:379–391
Pant D, Keefer CL (2009) Expression of pluripotency-related genes during bovine inner cell mass explant culture. Cloning Stem Cells 11:355–365
Puri G, Bag S, Das BC, Anees C, Nath NC, Majumdar AC (2010) Effect of different concentrations of serum supplementation on proliferation of embryonic cells derived from early stage in vitro buffalo embryos. Indian J Anim Sci 80:621–622
Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18:399–404
Rossant J (2007) Stem cells and lineage development in the mammalian blastocyst. Reprod Fertil Dev 19:111–118
Seamark RE (1994) Progress and emerging problems in livestock transgenesis: a summary perspective. Reprod Fertil Dev 6:653–657
Sharma GT, Dubey PK, Verma OP, Pratheesh MD, Nath A, Kumar GS (2012) Collagen-IV supported embryoid bodies formation and differentiation from buffalo (Bubalus bubalis) embryonic stem cells. Biochem Biophy Res Comm 424:378–384
Sharma M, Kumar R, Dubey PK, Verma OP, Nath A, Saikumar G, Sharma GT (2012) Expression and quantification of Oct-4 gene in blastocyst and embryonic stem cells derived from in vitro produced buffalo embryos. In Vitro Cell Dev Biol Anim 48:229–235
Sharma R, George A, Kamble NM, Singh KP, Chauhan MS, Singla SK, Manik RS, Palta P (2011) Optimization of culture conditions to support long-term self-renewal of buffalo (Bubalus bubalis) embryonic stem cell-like cells. Cell Reprogramming 13:539–549
Sharma R, George A, Kamble NM, Chauhan MS, Singla S, Manik RS, Palta P (2012) Growth factor expression pattern of homologous feeder layer for culturing buffalo embryonic stem cell-like cells. Reprod Fertil Dev 24:1098–1104
Singh J, Mann A, Kumar D, Duhan JS, Yadav PS (2013) Cultured buffalo umbilical cord matrix cells exhibit characteristics of multipotent mesenchymal stem cells. In Vitro Cell Dev Biol Anim 49:408–416
Singh KP, Kaushik R, Garg V, Sharma R, George A, Singh MK, Manik RS, Palta P, Singla SK, Chauhan MS (2012) Expression pattern of pluripotent markers in different embryonic developmental stages of buffalo (Bubalus bubalis) embryos and putative embryonic stem cells generated by parthenogenetic activation. Cell Reprogramming 14(6):530–538
Singh MK, Singh KP, Kumar D, Shah RA, Anand T, Chauhan MS, Manik RS, Singla SK, Palta P (2013) Buffalo (Bubalus bubalis) ES cell–like cells are capable of in vitro skeletal myogenic differentiation. Reprod Dom Anim 48:284–291
Smith SL, Everts RE, Tian XC, Du F, Sung LY, Rodriguez-Zas SL, Jeong BS, Renard JP, Lewin HA, Yang X (2005) Global gene expression profiles reveal significant nuclear reprogramming by the blastocyst stage after cloning. Proc Natl Acad Sci USA 102:17582–17587
Sritanaudomchai H, Pavasuthipasit K, Kitiyanant Y, Kupradinum P, Mitalipov S, Kusamran T (2007) Characterization and multilineage differentiation of embryonic stem cells derived from a buffalo parthenogenetic embryo. Mol Reprod Dev 74:1295–1302
Stice SL, Strelchenko N, Keefer CL, Matthews L (1996) Pluripotent bovine embryonic cell lines direct embryonic development following nuclear transfer. Biol Reprod 54:100–110
Strelchenko N (1996) Bovine pluripotent stem cells. Theriogenology 45:131–140
Talbot NC, Blomberg L (2008) The pursuit of ESC lines of domesticated ungulates. Stem Cell Rev 4:235–254
Tan T, Tang X, Zhang J, Niu Y, Chen H, Li B, Wei Q, Ji W (2011) Generation of trophoblast stem cells from rabbit embryonic stem cells with BMP4. PLoS One 17:e17124
Thomson JA, Itskovitzeldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147
Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA, Hearn JP (1995) Isolation of a primate embryonic stem-cell line. Proc Natl Acad Sci USA 92:7844–7848
Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR, Miller FD (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778–784
Totey SM, Daliri M, Appa-Rao KBC, Pawshe CH, Taneja M, Chillar RS (1996) Differential cleavage and developmental rates and their correlation with cell numbers and sex ratios in buffalo embryos generated in vitro. Theriogenology 45:521–533
Ueda S, Kawamata M, Teratani T, Shimizu T, Tamai Y, Ogawa H, Hayashi K, Tsuda H, Ochiya T (2008) Establishment of rat embryonic stem cells and making of chimera rats. PLoS One 30:e2800
Verma OP, Kumar R, Nath A, Sharma M, Dubey PK, Kumar GS, Sharma GT (2012) In vivo differentiation potential of buffalo (Bubalus bubalis) embryonic stem cell. In Vitro Cell Dev Biol Anim 48:349–358
Verma V, Guatam SK, Singh B, Manik RS, Palta P, Singla SK, Goswami SL, Chauhan MS (2007) Isolation and characterization of embryonic stem cell- like cells from in vitro produced buffalo (Bubalus bubalis) embryos. Mol Reprod Dev 74:520–529
Wang L, Duan E, Sung L, Jeong B, Yang X, Tian XC (2005) Generation and characterization of pluripotent stem cells from cloned bovine embryos. Biol Reprod 73:149–155
Wang S, Shen Y, Yuan X, Chen K, Guo X, Chen Y, Niu Y, Li J, Xu RH, Yan X, Zhou Q, Ji W (2008) Dissecting signalling pathways that govern self-renewal of rabbit embryonic stem cells. J Biol Chem 283:35929–35940
Wobus AM, Boheler KR (2005) Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 85:635–678
Wolf DP, Kuo H, Pau KF, Lester L (2004) Progress with nonhuman primate embryonic stem cells. Biol Reprod 71:1766–1771
Xie B, Qin Z, Huang B, Xie T, Yao H, Wei Y, Yang X, Shi D, Jiang H (2010) In vitro culture and differentiation of buffalo (Bubalus bubalis) spermatogonia. Reprod Domest Anim 45:275–282
Xu RH, Chen X, Li DS, Li R, Addicks GC, Glennon C, Zwaka TP, Thomson JA (2002) BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20:1261–1264
Yadav PS, Mann A, Singh J, Kumar D, Sharma RK, Singh I (2012) Buffalo (Bubalus bubalis) fetal skin derived fibroblast cells exhibit characteristics of stem cells. Agri Res 1:175–182
Yadav PS, Mann A, Singh V, Yashveer S, Sharma RK, Singh I (2011) Expression of pluripotency genes in buffalo (Bubalus bubalis) amniotic fluid cells. Reprod Dom Anim 46:705–711
Yadav PS, Singh RK, Singh B (2012) Fetal stem cells in farm animals: applications in health and production. Agric Res 1:67–77
Yang X, Kubota C, Suzuki H, Taneja M, Bols PE, Presicce GA (1998) Control of oocyte maturation in cows-biological factors. Theriogenology 49:471–482
Ying QL, Nichols J, Chambers I, Smith A (2003) BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115:281–292
Zandi M, Muzaffar M, Shah SM, Kaushik R, Singh MK, Palta P, Singla SK, Manik RS, Chauhan MS (2014) WNT3A signalling pathway in buffalo (Bubalus bubalis) embryonic stem cells. Reprod Fertil Dev 26:551–561
Zicarelli L, Di PR, Palladino M, Campanile G, Esposito L (1993) Embryo transfer in Mediterranean Bubalus bubalis. Proceedings of International Symposium on Prospects of Buffalo Production in the Mediterranean and the Middle East, Cairo, 9–12 Nov 1993: 73–75
Conflict of interest
Authors declare no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kumar, D., Anand, T., Lalaji, S.N. et al. Buffalo Embryonic, Fetal and Adult Stem Cells: Progress and Challenges. Agric Res 4, 7–20 (2015). https://doi.org/10.1007/s40003-014-0142-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40003-014-0142-6