|
|
|
|
|
| Transplantation of Goat Bone Marrow Mesenchymal Stem Cells (gMSCs) Help Restore Spermatogenesis in Endogenous Germ Cells-Depleted Mouse Models |
| WANG Fang, LIU Chao, ZHANG Shan-shan, LIU Wei-shuai , HUA Jin-lian |
1.College of Veterinary Medicine, Shaanxi Centre of Stem Cells Engineering and Technology, Northwest A&F University, Yangling 712100,P.R.China
2.Department of Pathology, Yangling Demonstration Zone Hospital, Yangling 712100, P.R.China |
|
|
|
摘要 Mesenchymal stem cells (MSCs) derived from bone marrow are a well-characterized population of adult stem cells that can be maintained and propagated in culture for a long time with the capacity to form a variety of cell types. This study investigated the characteristics of dairy goat bone marrow MSCs (gMSCs) and their differentiation potential toward germ cells in vitro, and to test their potential in vivo, these cells were transplanted into seminiferous tubes of endogenous germ cells-depleted mouse models. The results showed that characteristic gMSC lines were established and a small population of gMSCs transdifferentiated into male germ cell-like cells which expressed Stra8 after induction with retinoic acid (RA), as analysed by reverse transcription-polymerase chain reaction (RT-PCR) and immunofluorescence. Further, we transplanted the gMSCs into endogenous germ cells-depleted mouse models. A variety of analysis demonstrated that gMSCs might differentiate into male germ cells and helped spermatogenesis in endogenous germ cells depleted mouse models at 30 d after transplantation. The gMSCs could be used as a potential source of cells for reproductive studies and a neoadjuvant therapy for the spermatogenesis anomaly. Moreover, these cells may offer a new strategy for male infertility and an alternative approach for production of transgenic animals.
Abstract Mesenchymal stem cells (MSCs) derived from bone marrow are a well-characterized population of adult stem cells that can be maintained and propagated in culture for a long time with the capacity to form a variety of cell types. This study investigated the characteristics of dairy goat bone marrow MSCs (gMSCs) and their differentiation potential toward germ cells in vitro, and to test their potential in vivo, these cells were transplanted into seminiferous tubes of endogenous germ cells-depleted mouse models. The results showed that characteristic gMSC lines were established and a small population of gMSCs transdifferentiated into male germ cell-like cells which expressed Stra8 after induction with retinoic acid (RA), as analysed by reverse transcription-polymerase chain reaction (RT-PCR) and immunofluorescence. Further, we transplanted the gMSCs into endogenous germ cells-depleted mouse models. A variety of analysis demonstrated that gMSCs might differentiate into male germ cells and helped spermatogenesis in endogenous germ cells depleted mouse models at 30 d after transplantation. The gMSCs could be used as a potential source of cells for reproductive studies and a neoadjuvant therapy for the spermatogenesis anomaly. Moreover, these cells may offer a new strategy for male infertility and an alternative approach for production of transgenic animals.
|
|
Received: 13 September 2011
Accepted:
|
| Fund: This work was supported by the grants from the National Natural Science Foundation of China (30972097), the Key Program of Ministry of Education of China (109148), the Proram for New Century Excellent Talents in University, China (NCET-09-0654), the Scientific Research Program of Shaanxi Province, China (2011K02- 06), and the China Postdoctoral Science Foundation (20080431253). |
|
Corresponding Authors:
Correspondence HUA Jin-lian, Tel/Fax: +86-29-87080068, E-mail: jinlianhua@nwsuaf.edu.cn, Jlhua2003@126.com
E-mail: jinlianhua@nwsuaf.edu.cn, Jlhua2003@126.com
|
Cite this article:
WANG Fang, LIU Chao, ZHANG Shan-shan, LIU Wei-shuai , HUA Jin-lian.
2013.
Transplantation of Goat Bone Marrow Mesenchymal Stem Cells (gMSCs) Help Restore Spermatogenesis in Endogenous Germ Cells-Depleted Mouse Models. Journal of Integrative Agriculture, 12(3): 483-494.
|
| [1]Abrishami M, Anzar M, Yang Y, Honaramooz A. 2010.Cryopreservation of immature porcine testis tissue tomaintain its developmental potential after xenograftinginto recipient mice. Theriogenology, 73, 86-96[2]Abbasi S, Honaramooz A. 2011. The number of graftedfragments affects the outcome of testis tissuexenografting frompiglets into recipientmice. VeterinaryMedicine International, doi: 10.4061/2011/686570[3]Anderson E L, Baltus A E, Roepers-Gajadien H L, HassoldT J, de Rooij D G, van Pelt A M M, Page D C. 2008. Stra8and its inducer, retinoic acid, regulate meiotic initiationin both spermatogenesis and oogenesis in mice.Proceedings of the National Academy of Sciences ofthe United States of America, 105, 14976-14980[4]Brinster R L. 2002. Germline stem cell transplantation andransgenesis. Science, 296, 2174-2176[5]Brinster R L, Zimmermann J W 1994. Spermatogenesisfollowing male germ-cell transplantation. Proceedingsof the National Academy of Sciences of the UnitedStates of America, 91, 11298-11302[6]Cao H, Chu Y, Zhu H, Sun J, Pu Y, Gao Z, Yang C, Peng S,Dou Z, Hua J. 2011. Characterization of immortalizedmesenchymal stem cells derived from fetal porcinepancreas. Cell Proliferation, 44, 19-32[7]Clark A T, Bodnar M S, Fox M, Rodriquez R T, Abeyta M J,Firpo M T, Pera R A R. 2004. Spontaneous differentiationof germ cells from human embryonic stem cells in vitro.Human Molecular Genetics, 13, 727-739[8]Danner S, Kajahn J, Geismann C, Klink E, Kruse C. 2007.Derivation of oocyte-like cells from a clonal pancreaticstem cell line. Molecular Human Reproduction, 13, 11-20[9]Dobrinski I, Avarbock M R, Brinster R L. 2000. Germ celltransplantation from large domestic animals into mousetestes. Molecular Reproduction and Development, 57,270-279[10]Drusenheimer N, Wulf G, Nolte J, Lee J H, Dev A, DresselR, Gromoll J, Schmidtke J, Engel W, Nayernia K. 2007.Putative human male germ cells from bone marrow stemcells. Society of Reproduction and FertilitySupplement, 63, 69-76[11]Dyce P W, Wen L H, Li J L. 2006. In vitro germline potentialof stem cells derived from fetal porcine skin. NatureCell Biology, 8, 384-350[12]Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, DaleyG Q. 2004. Derivation of embryonic germ cells and malegametes from embryonic stem cells. Nature, 427,148-154[13]He Z, Jiang J, Hofmann M C, Dym M. 2007. Gfra1 silencingin mouse spermatogonial stem cells results in theirdifferentiation via the inactivation of ret tyrosine kinase.Biology of Reproduction, 77, 723-733[14]Hill J R, Dobrinski I. 2006. Male germ cell transplantation inlivestock. Reproduction, Fertility and Development,18, 13-18[15]Honaramooz A, Behboodi E, Megee S O, Overton S A,Galantino-Homer H, Echelard Y, Dobrinski I. 2003.Fertility and germline transmission of donor haplotypef o l l o w i n g g e r m c e l l t r a n s p l a n t a t i o n i nimmunocompetent goats. Biology of Reproduction, 69,1260-1264[16]Hua J L, Pan S H, Yang C R, Dong W Z, Dou Z Y, Sidhu KS. 2009. Derivation of male germ cell-like lineage fromhuman fetal bone marrow stern cells. ReproductiveBiomedicine Online, 19, 99-105[17]Hubner K, Fuhrmann G, Christenson L K, Kehler J, ReinboldR, de La Fuente R, Wood J, Strauss J F, Boiani M,Scholer H R. 2003. Derivation of oocytes from mouseembryonic stem cells. Science, 300, 1251-1256[18]Iammarrone E, Balet R, Gillott C, Grudzinskas J G. 2003.Male infertility. Best Practice & Research ClinicalObstetrics & Gynaecology, 17, 211-229[19]Izadyar F, Den Ouden K, Stout T A E, Stout J, Coret J,Lankveld D P K, Spoormakers T J P, Colenbrander B,Oldenbroek J K, van der Ploeg K D, et al. 2003.Autologous and homologous transplantation of bovinespermatogonial stem cells. Reproduction, 126, 765-774[20]Jiang Y H, Jahagirdar B N, Reinhardt R L, Schwartz R E,Keene C D, Ortiz-Gonzalez X R, Reyes M, Lenvik T,Lund T, Blackstad M, et al. 2002. Pluripotency ofmesenchymal stem cells derived from adult marrow.Nature, 418, 41-49[21]Kee K, Angeles V T, Flores M, Nguyen H N, Pera R A R.2009. Human DAZL, DAZ and BOULE genes modulateprimordial germ-cell and haploid gamete formation.Nature, 462, 222-225[22]Ko K, Tapia N, Wu G, Kim J B, Bravo M J A, Sasse P, GlaserT, Ruau D, Han DW, Greber B, et al. 2009. Induction ofpluripotency in adult unipotent germline stem cells. CellStem Cell, 5, 87-96[23]Koubova J, Menke D B, Zhou Q, Capel B, Griswold M D,Page D C. 2006. Retinoic acid regulates sex-specifictiming of meiotic initiation in mice. Proceedings of theNational Academy of Sciences of the United States ofAmerica, 103, 2474-2479[24]Lambard S, Galeraud-Denis I, Martin G, Levy R, Chocat A,Carreau S. 2004. Analysis and significance of mRNA inhuman ejaculated sperm from normozoospermic donors:relationship to sperm motility and capacitation.Molecular Human Reproduction, 10, 535-541[25]Lassalle B, Mouthon M A, Riou L, Barroca V, Coureuil M,Boussin F, Testart J, Allemand I, Fouchet P. 2008. Bonemarrow-derived stem cells do not reconstitutespermatogenesis in vivo. Stem Cells, 26, 1385-1386[26]Lee D R, Kim K S, Yang Y H, Oh H S, Lee S H, Chung T G,Cho J H, Kim H J, Yoon T K, Cha K Y. 2006. Isolation ofmale germ stem cell-like cells from testicular tissue ofnon-obstructive azoospermic patients anddifferentiation into haploid male germ cells in vitro.Human Reproduction, 21, 471-476[27]Li W, Dou Z, Hua J, Wang H. 2007. Activation of stra 8gene during the differentiation of spermatogonial stemcells. Chinese Journal of Biotechnology, 23, 639-644[28](in Chinese)Liu F H, Yang D Z, Wang Y F, Liang X P, Peng W M, Cao CA, Chen X G, Guo Z M. 2007. Mesenchymal stem cellsdo not differentiate into “quasi-sperm”. Zhonghua NanKe Xue, 13, 309-311 (in Chinese)[29]Lue Y, Erkkila K, Liu P Y, Ma K, Wang C, Hikim A S,Swerdloff R S. 2007. Fate of bone marrow stem cellstransplanted into the testis-potential implication for menwith testicular failure. American Journal of Pathology,170, 899-908[30]Mansouri A, Phi-van L, Geithe H P, Engel W. 1983.Proacrosin/acrosin activity during spermiohistogenesisof the bull. Differentiation, 24, 149-152[31]Nagano M, Brinster C J, Orwig K E, Ryu B Y, Avarbock MR, Brinster R L. 2001. Transgenic mice produced byretroviral transduction of male germ-line stem cells.Proceedings of the National Academy of Sciences ofthe United States of America, 98, 13090-13095[32]Nakai M, Kaneko H, Somfai T, Maedomari N, Ozawa M,Noguchi J, Ito J, Kashiwazaki N, Kikuchi K. 2010.Production of viable piglets for the first time using spermderived from ectopic testicular xenografts.Reproduction, 139, 331-335[33]Nayernia K, Lee J H, Drusenheimer N, Nolte J, Wulf G,Dressel R, Gromoll J, Engel W. 2006a. Derivation ofmale germ cells from bone marrow stem cells. LaboratoryInvestigation, 86, 654-663[34]Nayernia K, Li M Y, Jaroszynski L, Khusainov R, Wulf G,Schwandt I, Korabiowska M, Michelmann H W,Meinhardt A, Engel W. 2004. Stem cell basedtherapeutical approach of male infertility byteratocarcinoma derived germ cells. Human MolecularGenetics, 13, 1451-1460[35]Nayernia K, Nolte J, Michelmann H W, Lee J H, RathsackK, Drusenheimer N, Dev A, Wulf G, Ehrmann I E, ElliottD J, et al. 2006b. In vitro-differentiated embryonic stemcells give rise to male gametes that can generateoffspring mice. Developmental Cell, 11, 125-132[36]Oatley J M, de Avila D M, McLean D J, Griswold M D,Reeves J J. 2002. Transplantation of bovine germinalcells into mouse testes. Journal of Animal Science, 80,1925-1931[37]Oatley J M, Reeves J J, McLean D J. 2005. Establishment ofspermatogenesis in neonatal bovine testicular tissuefollowing ectopic xenografting varies with donor age.Biology of Reproduction, 72, 358-364[38]Ogawa T, Arechaga J M, Avarbock M R, Brinster R L. 1997.Transplantation of tesis germinal cells into mouseseminiferous tubules. International Journal ofDevelopment Biology, 41, 111-122[39]Oulad-Abdelghani M, Bouillet P, Decimo D, Gansmuller A,Heyberger S, Dolle P, Bronner S, Lutz Y, Chambon P.1996. Characterization of a premeiotic germ cell-specificcytoplasmic protein encoded by Stra8, a novel retinoicacid-responsive gene. Journal of Cell Biology, 135,469-477[40]Pawar S S, Malakar D, De A K, Akshey Y S. 2009. Stem celllikeoutgrowths from in vitro fertilized goat blastocysts.Indian Journal of Experiment Biology, 47, 635-642[41]Pittenger M F, Mackay A M, Beck S C, Jaiswal R K, DouglasR, Mosca J D, Moorman M A, Simonetti D W, Craig S,Marshak D R. 1999. Multilineage potential of adulthuman mesenchymal stem cells. Science, 284, 143-147[42]Rathi R, Honaramooz A, Zeng W, Turner R, Dobrinski I.2006. Germ cell development in equine testis tissuexenografted into mice. Reproduction, 131, 1091-1098[43]Revel A, Revel-Vilk S. 2010. Fertility preservation in youngcancer patients. Journal of Human ReproductiveSciences, 3, 2-7[44](in Chinese)Shao Z H, Wang P J, Li M H, Zhang W, Zheng S Q, Zhao XH, Wang G L, Shang M Y, Mao X Q. 2009. Effects ofmesenchymal stem cell transplantation on growth ofliver cancer: experiment with rats. Zhonghua Yi Xue ZaZhi, 89, 491-496[45](in Chinese)Shen F J, Zhang C, Zheng H Y, Xiong Y H, Wang X, Liao WB, Du X J, Yang S X, Wang L L. 2010. Long-term cultureand transplantation of spermatogonial stem cells fromBALB/c mice. Cells Tissues Organs, 191, 372-381[46]Toyooka Y, Tsunekawa N, Akasu R, Noce T. 2003.Embryonic stem cells can form germ cells in vitro.Proceedings of the National Academy of Sciences ofthe United States of America, 100, 11457-11462[47]Wang D Z, Zhou X H, Yuan Y L, Zheng X M. 2010. Optimaldose of busulfan for depleting testicular germ cells ofrecipient mice before spermatogonial transplantation.Asian Journal of Andrology, 12, 263-270[48]Yazawa T, Mizutani T, Yamada K, Kawata H, Sekiguchi T,Yoshino M, Kajitani T, Shou Z, Umezawa A, MiyamotoK. 2006. Differentiation of adult stem cells derived frombone marrow stroma into leydig or adrenocortical cells.Endocrinology, 147, 4104-4111[49]Yu F, Ding L J, Sun G B, Sun P X, He X H, Ni LG, Li B C.2 0 1 0 . T r a n s g e n i c s p e r m p r o d u c e d b yelectrotransfection and allogeneic transplantation ofchicken fetal spermatogonial stem cells. MolecularReproduction and Development, 77, 340-347[50]Zhang Z, Shao S, Shetty G, Meistrich M L. 2009. DonorSertoli cells transplanted into irradiated rat testesstimulate partial recovery of endogenousspermatogenesis. Reproduction, 137, 497-508[51]Zhang Y, Shen W, Hua J, Lei A, Lv C, Wang H, Yang C, GaoZ, Dou Z. 2010. Pancreatic islet-like clusters from bonemarrow mesenchymal stem cells of human first-trimesterabortus can cure streptozocin-induced mouse diabetes.Rejuvenation Research, 13, 695-706 |
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
