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Home / Equine Research Bank / J Assist Reprod Genet / Effect of intra-ovarian injection of mesenchymal stem cells ...
Journal of assisted reproduction and genetics2018; 36(3); 543-556; doi: 10.1007/s10815-018-1371-6

Effect of intra-ovarian injection of mesenchymal stem cells in aged mares.

Abstract: This study aims to determine if intra-ovarian injection of bone marrow-derived mesenchymal stem cells (MSCs) improves or restores ovarian function in aged females. Methods: Prospective randomized study of eight aged mares and six young mares receiving intra-ovarian injection of MSCs or vehicle. Main outcome measures were antral follicle count and serum anti-Müllerian hormone (AMH) (aged and young mares), and for aged mares, oocyte meiotic and developmental competence; gross and histological ovarian assessment; evaluation of presence of chimerism in recovered granulosa cells and in ovarian tissue samples; and gene expression in ovarian tissue as assessed by RNA sequencing. Results: Injection of MSCs was not associated with significant changes in follicle number, oocyte recovery rate on follicle aspiration, oocyte maturation rate, or blastocyst rate after ICSI in aged mares, or in changes in follicle number in young mares. There were no significant changes in peripheral AMH concentrations, indicating a lack of effect on growing follicles. MSC donor DNA was not recovered in granulosa cells or in ovarian tissue, indicating lack of persistence of injected MSC. RNA sequencing revealed significant differences in gene expression between MSC- and vehicle-injected ovaries. Conclusions: Intra-ovarian injection of bone marrow-derived MSCs altered gene expression but did not improve ovarian function in aged mares.
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Publication Date: 2018-11-23 PubMed ID: 30470961PubMed Central: PMC6439078DOI: 10.1007/s10815-018-1371-6Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article investigates whether injecting bone marrow-derived mesenchymal stem cells (MSCs) into the ovaries can enhance or restore ovarian function in older females, using mares as a model.

Study Design and Participants

  • The study was a prospective randomized trial involving fourteen mares divided into two age groups; old and young.
  • Both groups were subject to injections in their ovaries, either with MSCs or a vehicle (control).
  • The primary outcome measures included the count of antral follicles (small, fluid-filled sacs inside the ovary where eggs develop) and the level of serum anti-Müllerian hormone (AMH), an indicator of ovarian reserve.
  • For the older mares, additional criteria included the ability of their oocytes (eggs) to undergo meiosis (cell division) and develop properly, a thorough analysis of their ovaries visually and under the microscope, and the assessment of gene expression via RNA sequencing.

Study Findings

  • MSC injections didn’t significantly affect the number of antral follicles, the rate of oocyte retrieval, the rate of oocyte maturation, or the rate at which fertilized eggs developed into blastocysts in older mares.
  • There were also no significant changes in the number of follicles observed in younger mares.
  • Peripheral AMH concentrations remained stable, suggesting that the treatment didn’t impact growing follicles.
  • In a further blow to the effectiveness of the treatment, MSC donor DNA wasn’t detected in either the granulosa cells (the cells surrounding the egg in a follicle) or ovarian tissue samples, indicating these injected cells did not persist.
  • However, analysis of RNA sequences did show significant differences in gene expression between ovaries treated with MSCs and those injected with the vehicle, hinting at potential cellular changes stimulated by the treatment.

Study Conclusion

  • The study concluded that while the intra-ovarian injection of bone marrow-derived MSCs altered the gene expression within the ovaries, it did not improve ovarian function in the aged mares.

In other words, while the treatment had some effect on the ovaries at the molecular level, it did not result in any practical improvements in ovarian function or egg development required for fertility.

Cite This Article

APA
Grady ST, Watts AE, Thompson JA, Penedo MCT, Konganti K, Hinrichs K. (2018). Effect of intra-ovarian injection of mesenchymal stem cells in aged mares. J Assist Reprod Genet, 36(3), 543-556. https://doi.org/10.1007/s10815-018-1371-6

Publication

Journal of assisted reproduction and genetics
ISSN: 1573-7330
NlmUniqueID: 9206495
Country: Netherlands
Language: English
Volume: 36
Issue: 3
Pages: 543-556

Researcher Affiliations

Grady, Sicilia T
  • Department of Veterinary Physiology and Pharmacology, Texas A&M University, College Station, TX, 77843-4466, USA.
Watts, Ashlee E
  • Department of Large Animal Clinical Sciences, Texas A&M University, College Station, TX, 77843-4475, USA.
Thompson, James A
  • Department of Large Animal Clinical Sciences, Texas A&M University, College Station, TX, 77843-4475, USA.
Penedo, M Cecilia T
  • Veterinary Genetics Laboratory, University of California, Davis, CA, 95616, USA.
Konganti, Kranti
  • Texas A&M Institute for Genome Sciences and Society, Texas A&M University, College Station, TX, 77843, USA.
Hinrichs, Katrin
  • Department of Veterinary Physiology and Pharmacology, Texas A&M University, College Station, TX, 77843-4466, USA. khinrichs@cvm.tamu.edu.
  • Department of Large Animal Clinical Sciences, Texas A&M University, College Station, TX, 77843-4475, USA. khinrichs@cvm.tamu.edu.

MeSH Terms

  • Animals
  • Estradiol / metabolism
  • Female
  • Granulosa Cells / transplantation
  • Horses
  • Mesenchymal Stem Cell Transplantation
  • Mesenchymal Stem Cells / cytology
  • Oocyte Retrieval
  • Oocytes / growth & development
  • Ovarian Follicle / growth & development
  • Ovary / growth & development
  • Prospective Studies
  • Sequence Analysis, RNA

Grant Funding

  • NA / College of Veterinary Medicine & Biomedical Sciences, Texas A and M University

Conflict of Interest Statement

The authors declare that they have no conflict of interest.

References

This article includes 60 references
  1. Itay S, Abramovici A, Nevo Z. Use of cultured embryonal chick epiphyseal chondrocytes as grafts for defects in chick articular cartilage.. Clin Orthop Relat Res 1987 Jul;(220):284-303.
    pubmed: 3595003
  2. Wilke MM, Nydam DV, Nixon AJ. Enhanced early chondrogenesis in articular defects following arthroscopic mesenchymal stem cell implantation in an equine model.. J Orthop Res 2007 Jul;25(7):913-25.
    doi: 10.1002/jor.20382pubmed: 17405160google scholar: lookup
  3. Lee RH, Seo MJ, Reger RL, Spees JL, Pulin AA, Olson SD, Prockop DJ. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice.. Proc Natl Acad Sci U S A 2006 Nov 14;103(46):17438-43.
    doi: 10.1073/pnas.0608249103pmc: PMC1634835pubmed: 17088535google scholar: lookup
  4. Phinney DG, Isakova I. Plasticity and therapeutic potential of mesenchymal stem cells in the nervous system.. Curr Pharm Des 2005;11(10):1255-65.
    doi: 10.2174/1381612053507495pubmed: 15853682google scholar: lookup
  5. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects.. Proc Natl Acad Sci U S A 2003 Jul 8;100(14):8407-11.
    doi: 10.1073/pnas.1432929100pmc: PMC166242pubmed: 12815096google scholar: lookup
  6. Minguell JJ, Erices A. Mesenchymal stem cells and the treatment of cardiac disease.. Exp Biol Med (Maywood) 2006 Jan;231(1):39-49.
    doi: 10.1177/153537020623100105pubmed: 16380643google scholar: lookup
  7. Salooja N, Szydlo RM, Socie G, Rio B, Chatterjee R, Ljungman P, Van Lint MT, Powles R, Jackson G, Hinterberger-Fischer M, Kolb HJ, Apperley JF. Pregnancy outcomes after peripheral blood or bone marrow transplantation: a retrospective survey.. Lancet 2001 Jul 28;358(9278):271-6.
    doi: 10.1016/S0140-6736(01)05482-4pubmed: 11498213google scholar: lookup
  8. Sanders JE, Buckner CD, Amos D, Levy W, Appelbaum FR, Doney K, Storb R, Sullivan KM, Witherspoon RP, Thomas ED. Ovarian function following marrow transplantation for aplastic anemia or leukemia.. J Clin Oncol 1988 May;6(5):813-8.
    doi: 10.1200/JCO.1988.6.5.813pubmed: 3130466google scholar: lookup
  9. Sanders JE, Hawley J, Levy W, Gooley T, Buckner CD, Deeg HJ, Doney K, Storb R, Sullivan K, Witherspoon R, Appelbaum FR. Pregnancies following high-dose cyclophosphamide with or without high-dose busulfan or total-body irradiation and bone marrow transplantation.. Blood 1996 Apr 1;87(7):3045-52.
    pubmed: 8639928
  10. Takehara Y, Yabuuchi A, Ezoe K, Kuroda T, Yamadera R, Sano C, Murata N, Aida T, Nakama K, Aono F, Aoyama N, Kato K, Kato O. The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function.. Lab Invest 2013 Feb;93(2):181-93.
    doi: 10.1038/labinvest.2012.167pmc: PMC3561594pubmed: 23212100google scholar: lookup
  11. Wang S, Yu L, Sun M, Mu S, Wang C, Wang D, Yao Y. The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure.. Biomed Res Int 2013;2013:690491.
    pmc: PMC3753743pubmed: 23998127doi: 10.1155/2013/690491google scholar: lookup
  12. Lee HJ, Selesniemi K, Niikura Y, Niikura T, Klein R, Dombkowski DM, Tilly JL. Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure.. J Clin Oncol 2007 Aug 1;25(22):3198-204.
    doi: 10.1200/JCO.2006.10.3028pubmed: 17664466google scholar: lookup
  13. Fu X, He Y, Xie C, Liu W. Bone marrow mesenchymal stem cell transplantation improves ovarian function and structure in rats with chemotherapy-induced ovarian damage.. Cytotherapy 2008;10(4):353-63.
    doi: 10.1080/14653240802035926pubmed: 18574768google scholar: lookup
  14. Mohammed Ali AF. Fertility treatment of aged women by laparoscopic intra ovarian injection of peripheral blood mononuclear cell (PBMNC) a new modality.. Fertil Mag 2013;52–5.
  15. Herraiz S, Romeu M, Buigues A, Martínez S, Díaz-García C, Gómez-Seguí I, Martínez J, Pellicer N, Pellicer A. Autologous stem cell ovarian transplantation to increase reproductive potential in patients who are poor responders.. Fertil Steril 2018 Aug;110(3):496-505.e1.
    doi: 10.1016/j.fertnstert.2018.04.025pubmed: 29960701google scholar: lookup
  16. Li J, Mao Q, He J, She H, Zhang Z, Yin C. Human umbilical cord mesenchymal stem cells improve the reserve function of perimenopausal ovary via a paracrine mechanism.. Stem Cell Res Ther 2017 Mar 9;8(1):55.
    doi: 10.1186/s13287-017-0514-5pmc: PMC5345137pubmed: 28279229google scholar: lookup
  17. Carnevale EM, Ginther OJ. Defective oocytes as a cause of subfertility in old mares.. Biol Reprod 1995;Monograph 1:209–214.
    doi: 10.1093/biolreprod/52.monograph_series1.209google scholar: lookup
  18. Fitzgerald C, Zimon AE, Jones EE. Aging and reproductive potential in women.. Yale J Biol Med 1998 Sep-Oct;71(5):367-81.
    pmc: PMC2578931pubmed: 10527364
  19. Colleoni S, Barbacini S, Necchi D, Duchi R, Lazzari G, Galli C. Application of ovum pick-up, intracytoplasmic sperm injection and embryo culture in equine practice.. Proc Am Assoc Equine Pract 2007;53:554–559.
  20. Jacobson CC, Choi YH, Hayden SS, Hinrichs K. Recovery of mare oocytes on a fixed biweekly schedule, and resulting blastocyst formation after intracytoplasmic sperm injection.. Theriogenology 2010 May;73(8):1116-26.
    doi: 10.1016/j.theriogenology.2010.01.013pubmed: 20202674google scholar: lookup
  21. Sellon DC. How to obtain a diagnostic bone marrow sample from the sternum of an adult horse.. Proc Am Assoc Equine Pract 2006;52:621–625.
  22. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.. Cytotherapy 2006;8(4):315-7.
    doi: 10.1080/14653240600855905pubmed: 16923606google scholar: lookup
  23. De Schauwer C, Piepers S, Van de Walle GR, Demeyere K, Hoogewijs MK, Govaere JL, Braeckmans K, Van Soom A, Meyer E. In search for cross-reactivity to immunophenotype equine mesenchymal stromal cells by multicolor flow cytometry.. Cytometry A 2012 Apr;81(4):312-23.
    doi: 10.1002/cyto.a.22026pubmed: 22411893google scholar: lookup
  24. Schnabel LV, Pezzanite LM, Antczak DF, Felippe MJ, Fortier LA. Equine bone marrow-derived mesenchymal stromal cells are heterogeneous in MHC class II expression and capable of inciting an immune response in vitro.. Stem Cell Res Ther 2014 Jan 24;5(1):13.
    doi: 10.1186/scrt402pmc: PMC4055004pubmed: 24461709google scholar: lookup
  25. Mitchell A, Rivas KA, Smith R 3rd, Watts AE. Cryopreservation of equine mesenchymal stem cells in 95% autologous serum and 5% DMSO does not alter post-thaw growth or morphology in vitro compared to fetal bovine serum or allogeneic serum at 20 or 95% and DMSO at 10 or 5.. Stem Cell Res Ther 2015 Nov 26;6:231.
    doi: 10.1186/s13287-015-0230-ypmc: PMC4661990pubmed: 26611913google scholar: lookup
  26. Brück I, Raun K, Synnestvedt B, Greve T. Follicle aspiration in the mare using a transvaginal ultrasound-guided technique.. Equine Vet J 1992 Jan;24(1):58-9.
    doi: 10.1111/j.2042-3306.1992.tb02780.xpubmed: 1555542google scholar: lookup
  27. Choi YH, Ross P, Velez IC, Macías-García B, Riera FL, Hinrichs K. Cell lineage allocation in equine blastocysts produced in vitro under varying glucose concentrations.. Reproduction 2015 Jul;150(1):31-41.
    doi: 10.1530/REP-14-0662pubmed: 25852156google scholar: lookup
  28. Choi YH, Love LB, Varner DD, Hinrichs K. Holding immature equine oocytes in the absence of meiotic inhibitors: effect on germinal vesicle chromatin and blastocyst development after intracytoplasmic sperm injection.. Theriogenology 2006 Sep 1;66(4):955-63.
    doi: 10.1016/j.theriogenology.2006.01.064pubmed: 16574209google scholar: lookup
  29. Rowland AL, Glass KG, Grady ST, Cummings KJ, Hinrichs K, Watts AE. Influence of caudal epidural analgesia on cortisol concentrations and pain-related behavioral responses in mares during and after ovariectomy via colpotomy.. Vet Surg 2018 Jul;47(5):715-721.
    doi: 10.1111/vsu.12908pubmed: 29774961google scholar: lookup
  30. Alves KA, Alves BG, Rocha CD, Visonná M, Mohallem RF, Gastal MO, Jacomini JO, Beletti ME, Figueiredo JR, Gambarini ML, Gastal EL. Number and density of equine preantral follicles in different ovarian histological section thicknesses.. Theriogenology 2015 Apr 1;83(6):1048-55.
    doi: 10.1016/j.theriogenology.2014.12.004pubmed: 25628263google scholar: lookup
  31. van de Goor LH, Panneman H, van Haeringen WA. A proposal for standardization in forensic equine DNA typing: allele nomenclature for 17 equine-specific STR loci.. Anim Genet 2010 Apr;41(2):122-7.
    doi: 10.1111/j.1365-2052.2009.01975.xpubmed: 19821810google scholar: lookup
  32. Bowling AT, Del Valle A, Bowling M. A pedigree-based study of mitochondrial D-loop DNA sequence variation among Arabian horses.. Anim Genet 2000 Feb;31(1):1-7.
    doi: 10.1046/j.1365-2052.2000.00558.xpubmed: 10690354google scholar: lookup
  33. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
    pmc: PMC4103590pubmed: 24695404doi: 10.1093/bioinformatics/btu170google scholar: lookup
  34. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements.. Nat Methods 2015 Apr;12(4):357-60.
    doi: 10.1038/nmeth.3317pmc: PMC4655817pubmed: 25751142google scholar: lookup
  35. Anders S, Pyl PT, Huber W. HTSeq--a Python framework to work with high-throughput sequencing data.. Bioinformatics 2015 Jan 15;31(2):166-9.
    pmc: PMC4287950pubmed: 25260700doi: 10.1093/bioinformatics/btu638google scholar: lookup
  36. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  37. Zhang JL. Comparative investigation of three Bayesian p values.. Comput Stat Data Anal 2014;79:277–291.
    doi: 10.1016/j.csda.2014.05.012google scholar: lookup
  38. Hinrichs K, Schmidt AL. Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season.. Biol Reprod 2000 May;62(5):1402-8.
    doi: 10.1095/biolreprod62.5.1402pubmed: 10775193google scholar: lookup
  39. Velez IC, Arnold C, Jacobson CC, Norris JD, Choi YH, Edwards JF, Hayden SS, Hinrichs K. Effects of repeated transvaginal aspiration of immature follicles on mare health and ovarian status.. Equine Vet J Suppl 2012 Dec;(43):78-83.
    doi: 10.1111/j.2042-3306.2012.00606.xpubmed: 23447883google scholar: lookup
  40. Duchamp G, Bézard J, Palmer E. Oocyte yield and the consequences of puncture of all follicles larger than 8 millimetres in mares.. Biol Reprod 1995;Monograph 1:233–241.
    doi: 10.1093/biolreprod/52.monograph_series1.233google scholar: lookup
  41. Abd-Allah SH, Shalaby SM, Pasha HF, El-Shal AS, Raafat N, Shabrawy SM, Awad HA, Amer MG, Gharib MA, El Gendy EA, Raslan AA, El-Kelawy HM. Mechanistic action of mesenchymal stem cell injection in the treatment of chemically induced ovarian failure in rabbits.. Cytotherapy 2013 Jan;15(1):64-75.
    doi: 10.1016/j.jcyt.2012.08.001pubmed: 23260087google scholar: lookup
  42. Ghadami M, El-Demerdash E, Zhang D, Salama SA, Binhazim AA, Archibong AE, Chen X, Ballard BR, Sairam MR, Al-Hendy A. Bone marrow transplantation restores follicular maturation and steroid hormones production in a mouse model for primary ovarian failure.. PLoS One 2012;7(3):e32462.
    doi: 10.1371/journal.pone.0032462pmc: PMC3296713pubmed: 22412875google scholar: lookup
  43. Rosen C, Shezen E, Aronovich A, Klionsky YZ, Yaakov Y, Assayag M, Biton IE, Tal O, Shakhar G, Ben-Hur H, Shneider D, Vaknin Z, Sadan O, Evron S, Freud E, Shoseyov D, Wilschanski M, Berkman N, Fibbe WE, Hagin D, Hillel-Karniel C, Krentsis IM, Bachar-Lustig E, Reisner Y. Preconditioning allows engraftment of mouse and human embryonic lung cells, enabling lung repair in mice.. Nat Med 2015 Aug;21(8):869-79.
    doi: 10.1038/nm.3889pubmed: 26168294google scholar: lookup
  44. Schnabel LV, Lynch ME, van der Meulen MC, Yeager AE, Kornatowski MA, Nixon AJ. Mesenchymal stem cells and insulin-like growth factor-I gene-enhanced mesenchymal stem cells improve structural aspects of healing in equine flexor digitorum superficialis tendons.. J Orthop Res 2009 Oct;27(10):1392-8.
    doi: 10.1002/jor.20887pubmed: 19350658google scholar: lookup
  45. Iso Y, Spees JL, Serrano C, Bakondi B, Pochampally R, Song YH, Sobel BE, Delafontaine P, Prockop DJ. Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment.. Biochem Biophys Res Commun 2007 Mar 16;354(3):700-6.
    doi: 10.1016/j.bbrc.2007.01.045pmc: PMC1851899pubmed: 17257581google scholar: lookup
  46. Spees JL, Olson SD, Whitney MJ, Prockop DJ. Mitochondrial transfer between cells can rescue aerobic respiration.. Proc Natl Acad Sci U S A 2006 Jan 31;103(5):1283-8.
    doi: 10.1073/pnas.0510511103pmc: PMC1345715pubmed: 16432190google scholar: lookup
  47. Claes A, Ball BA, Scoggin KE, Esteller-Vico A, Kalmar JJ, Conley AJ, Squires EL, Troedsson MH. The interrelationship between anti-Müllerian hormone, ovarian follicular populations and age in mares.. Equine Vet J 2015 Sep;47(5):537-41.
    pubmed: 25124401doi: 10.1111/evj.12328google scholar: lookup
  48. Behnam B, Modarressi MH, Conti V, Taylor KE, Puliti A, Wolfe J. Expression of Tsga10 sperm tail protein in embryogenesis and neural development: from cilium to cell division.. Biochem Biophys Res Commun 2006 Jun 16;344(4):1102-10.
    doi: 10.1016/j.bbrc.2006.03.240pubmed: 16643851google scholar: lookup
  49. Mobasheri MB, Jahanzad I, Mohagheghi MA, Aarabi M, Farzan S, Modarressi MH. Expression of two testis-specific genes, TSGA10 and SYCP3, in different cancers regarding to their pathological features.. Cancer Detect Prev 2007;31(4):296-302.
    doi: 10.1016/j.cdp.2007.05.002pubmed: 17920210google scholar: lookup
  50. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, Yefanov A, Lee H, Zhang N, Robertson CL, Serova N, Davis S, Soboleva A. NCBI GEO: archive for functional genomics data sets--update.. Nucleic Acids Res 2013 Jan;41(Database issue):D991-5.
    doi: 10.1093/nar/gks1193pmc: PMC3531084pubmed: 23193258google scholar: lookup
  51. Small CL, Shima JE, Uzumcu M, Skinner MK, Griswold MD. Profiling gene expression during the differentiation and development of the murine embryonic gonad.. Biol Reprod 2005 Feb;72(2):492-501.
    doi: 10.1095/biolreprod.104.033696pmc: PMC3217241pubmed: 15496517google scholar: lookup
  52. Kenigsberg S, Bentov Y, Chalifa-Caspi V, Potashnik G, Ofir R, Birk OS. Gene expression microarray profiles of cumulus cells in lean and overweight-obese polycystic ovary syndrome patients.. Mol Hum Reprod 2009 Feb;15(2):89-103.
    doi: 10.1093/molehr/gan082pubmed: 19141487google scholar: lookup
  53. Miryounesi M, Nayernia K, Mobasheri MB, Dianatpour M, Oko R, Savad S, Modarressi MH. Evaluation of in vitro spermatogenesis system effectiveness to study genes behavior: monitoring the expression of the testis specific 10 (Tsga10) gene as a model.. Arch Iran Med 2014 Oct;17(10):692-7.
    pubmed: 25305769
  54. Tanaka R, Ono T, Sato S, Nakada T, Koizumi F, Hasegawa K, Nakagawa K, Okumura H, Yamashita T, Ohtsuka M, Asagoe K, Yamasaki O, Noguchi Y, Iwatsuki K, Nakayama E. Over-expression of the testis-specific gene TSGA10 in cancers and its immunogenicity.. Microbiol Immunol 2004;48(4):339-45.
    doi: 10.1111/j.1348-0421.2004.tb03515.xpubmed: 15107545google scholar: lookup
  55. Volodko N, Gordon M, Salla M, Ghazaleh HA, Baksh S. RASSF tumor suppressor gene family: biological functions and regulation.. FEBS Lett 2014 Aug 19;588(16):2671-84.
    doi: 10.1016/j.febslet.2014.02.041pubmed: 24607545google scholar: lookup
  56. Lee CM, Yang P, Chen LC, Chen CC, Wu SC, Cheng HY, Chang YS. A novel role of RASSF9 in maintaining epidermal homeostasis.. PLoS One 2011 Mar 21;6(3):e17867.
    doi: 10.1371/journal.pone.0017867pmc: PMC3061870pubmed: 21445300google scholar: lookup
  57. Mashaghi A, Marmalidou A, Tehrani M, Grace PM, Pothoulakis C, Dana R. Neuropeptide substance P and the immune response.. Cell Mol Life Sci 2016 Nov;73(22):4249-4264.
    doi: 10.1007/s00018-016-2293-zpmc: PMC5056132pubmed: 27314883google scholar: lookup
  58. Ziche M, Morbidelli L, Pacini M, Geppetti P, Alessandri G, Maggi CA. Substance P stimulates neovascularization in vivo and proliferation of cultured endothelial cells.. Microvasc Res 1990 Sep;40(2):264-78.
    doi: 10.1016/0026-2862(90)90024-Lpubmed: 1701206google scholar: lookup
  59. Ahmad M, Srinivasula SM, Wang L, Talanian RV, Litwack G, Fernandes-Alnemri T, Alnemri ES. CRADD, a novel human apoptotic adaptor molecule for caspase-2, and FasL/tumor necrosis factor receptor-interacting protein RIP.. Cancer Res 1997 Feb 15;57(4):615-9.
    pubmed: 9044836
  60. Joswig AJ, Mitchell A, Cummings KJ, Levine GJ, Gregory CA, Smith R 3rd, Watts AE. Repeated intra-articular injection of allogeneic mesenchymal stem cells causes an adverse response compared to autologous cells in the equine model.. Stem Cell Res Ther 2017 Feb 28;8(1):42.
    doi: 10.1186/s13287-017-0503-8pmc: PMC5329965pubmed: 28241885google scholar: lookup

Citations

This article has been cited 17 times.
  1. Wang Y, Jin C, Yi Y, Hu Y, Han X, Tan Z, Wang Z, Kang J. Rumen-protected glucose stimulates the secretion of reproductive hormones and the mTOR/AKT signaling pathway in the ovaries of early postpartum. Sci Rep 2023 Feb 20;13(1):2940.
    doi: 10.1038/s41598-023-30170-5pubmed: 36808140google scholar: lookup
  2. Saeed Y, Liu X. Mesenchymal stem cells to treat female infertility; future perspective and challenges: A review. Int J Reprod Biomed 2022 Sep;20(9):709-722.
    doi: 10.18502/ijrm.v20i9.12061pubmed: 36340664google scholar: lookup
  3. Mawet M, Perrier d'Hauterive S, Henry L, Potorac I, Kridelka F, Nisolle M, Pintiaux A. Restoration of Fertility in Patients with Spontaneous Premature Ovarian Insufficiency: New Techniques under the Microscope. J Clin Med 2021 Nov 30;10(23).
    doi: 10.3390/jcm10235647pubmed: 34884349google scholar: lookup
  4. Gomes EM, Dos Santos EAP, Neto LFL, Padilha DR, Campos GCS, Thiesen R, Machado IRL, Mestieri MLA. Transcutaneous Ultrasound Guided Intraovarian Injection in Rats (Rattus norvegicus). J Am Assoc Lab Anim Sci 2021 Sep 1;60(5):502-505.
    doi: 10.30802/AALAS-JAALAS-20-000136pubmed: 34281630google scholar: lookup
  5. Petric P, Vrtacnik-Bokal E, Stimpfel M. Is It Possible to Treat Infertility with Stem Cells?. Reprod Sci 2021 Jun;28(6):1733-1745.
    doi: 10.1007/s43032-021-00566-7pubmed: 33834375google scholar: lookup
  6. Cequier A, Sanz C, Rodellar C, Barrachina L. The Usefulness of Mesenchymal Stem Cells beyond the Musculoskeletal System in Horses. Animals (Basel) 2021 Mar 25;11(4).
    doi: 10.3390/ani11040931pubmed: 33805967google scholar: lookup
  7. Voga M, Adamic N, Vengust M, Majdic G. Stem Cells in Veterinary Medicine-Current State and Treatment Options. Front Vet Sci 2020;7:278.
    doi: 10.3389/fvets.2020.00278pubmed: 32656249google scholar: lookup
  8. Na J, Kim GJ. Recent trends in stem cell therapy for premature ovarian insufficiency and its therapeutic potential: a review. J Ovarian Res 2020 Jun 23;13(1):74.
    doi: 10.1186/s13048-020-00671-2pubmed: 32576209google scholar: lookup
  9. Malard PF, Peixer MAS, Grazia JG, Brunel HDSS, Feres LF, Villarroel CL, Siqueira LGB, Dode MAN, Pogue R, Viana JHM, Carvalho JL. Intraovarian injection of mesenchymal stem cells improves oocyte yield and in vitro embryo production in a bovine model of fertility loss. Sci Rep 2020 May 15;10(1):8018.
    doi: 10.1038/s41598-020-64810-xpubmed: 32415089google scholar: lookup
  10. Reig A, Mamillapalli R, Coolidge A, Johnson J, Taylor HS. Uterine Cells Improved Ovarian Function in a Murine Model of Ovarian Insufficiency. Reprod Sci 2019 Dec;26(12):1633-1639.
    doi: 10.1177/1933719119875818pubmed: 31530098google scholar: lookup
  11. Yoon SY. Mesenchymal stem cells for restoration of ovarian function. Clin Exp Reprod Med 2019 Mar;46(1):1-7.
    doi: 10.5653/cerm.2019.46.1.1pubmed: 30827071google scholar: lookup
  12. Aboutalebi H, Vafaei S, Aboutalebi M, Dortaj H, Alipour F, Bideskan AE. Premature ovarian insufficiency restoration after chemotherapy: current achievements and future prospects on its treatment or management. J Ovarian Res 2025 Jul 31;18(1):171.
    doi: 10.1186/s13048-025-01677-4pubmed: 40745328google scholar: lookup
  13. Cui X, Jing X. Stem cell-based therapeutic potential in female ovarian aging and infertility. J Ovarian Res 2024 Aug 24;17(1):171.
    doi: 10.1186/s13048-024-01492-3pubmed: 39182123google scholar: lookup
  14. Kim HK, Kim TJ. Current Status and Future Prospects of Stem Cell Therapy for Infertile Patients with Premature Ovarian Insufficiency. Biomolecules 2024 Feb 19;14(2).
    doi: 10.3390/biom14020242pubmed: 38397479google scholar: lookup
  15. Ren W, Wang J, Zeng Y, Wang T, Meng J, Yao X. Differential age-related transcriptomic analysis of ovarian granulosa cells in Kazakh horses. Front Endocrinol (Lausanne) 2024;15:1346260.
    doi: 10.3389/fendo.2024.1346260pubmed: 38352714google scholar: lookup
  16. Cacciottola L, Vitale F, Donnez J, Dolmans MM. Use of mesenchymal stem cells to enhance or restore fertility potential: a systematic review of available experimental strategies. Hum Reprod Open 2023;2023(4):hoad040.
    doi: 10.1093/hropen/hoad040pubmed: 37954935google scholar: lookup
  17. Baouche M, Ochota M, Mermillod P, Locatelli Y, Nizanski W. Feline Wharton's jelly-derived mesenchymal stem cells as a feeder layer for oocytes maturation and embryos culture in vitro. Front Vet Sci 2023;10:1252484.
    doi: 10.3389/fvets.2023.1252484pubmed: 37869498google scholar: lookup
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