The impact of high hydrostatic pressure (40 MPa and 60 MPa) on the apoptosis rates and functional activity of cryopreserved porcine mesenchymal stem cells

Open access

Abstract

The aim of the present study was to examine the influence of two varied high hydrostatic pressure (HHP) values on the apoptosis (assessing caspase-8, survivin, CAD, Bax, BclxL and BclxS) and functional activity (using cocultures with bovine embryos) of porcine mesenchymal stem cells (pBMSCs). pBMSCs were isolated from porcine bone marrow and cultured in vitro. Before cryopreservation and storage in liquid nitrogen, pBMSCs were subjected to HHP values of 40 MPa and 60 MPa for 1 h at 24°C. After thawing, the cells were analysed for caspase-8 activity and protein expression of survivin, CAD, Bax, BclxL and BclxS. To indirectly test the influence of HHP on the functional activity of pBMSCs, in vitro maturated bovine oocytes were fertilized in vitro, and the obtained embryos were cultured under 4 different conditions: 1. monoculture in SOF medium; 2. coculture with pBMSCs in SOF medium; 3. coculture with pBMSCs subjected to 40 MPa HHP in SOF medium and 4. coculture with pBMSCs subjected to 60 MPa HHP in SOF medium. The quality of the developed blastocysts was analysed by TUNEL assay. HHP did not induce apoptosis in pBMSCs, as no significant difference was noted in the expression of any of the analysed apoptosis- related proteins between pBMSCs subjected to HHP (40 MPa or 60 MPa) and control. The highest number of obtained blastocysts was observed when the embryos were cultured in SOF. A highly significant difference (P<0.005) was noted between embryos cultured in SOF and embryos cultured in the presence of pBMSCs subjected to 60 MPa HHP or untreated pBMSCs. A significant difference (P<0.05) was noted between embryos cultured in SOF and embryos cultured in the presence of pBMSCs subjected to 40 MPa HHP. In conclusion, HHP does not induce apoptosis in pBMSCs. The obtained results of the blastocysts cocultured in vitro with pBMSCs (HHP-treated and untreated cells) imply that coculture with pBMSCs has a negative impact on the developmental rates of blastocysts.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Arno A.I. Amini- Nik S. Blit P.H. Al- Shehab M. Belo C. Herer E. Jeschke M.G. (2014). Effect of human Wharton’s jelly mesenchymal stem cell paracrine signaling on keloid fibroblasts. Stem Cells Transl. Med. 3: 299-307.

  • Atsuta I. Liu S. Miura Y. Akiyama K. Chen C. An Y. Shi S. Chen F.M. (2013). Mesenchymal stem cells inhibit multiple myeloma cells via the Fas/Fas ligand pathway. Stem Cell Res. Ther. 4: 111.

  • Bogliolo L. Ariu F. Leoni G. Uccheddu S. Bebbere D. (2011). High hydrostatic pressure treatment improves the quality of in vitro-produced ovine blastocysts. Reprod. Fertil. Dev. 23: 809-817.

  • Bourin P. Gadelorge M. Peyrafitte J.A. Fleury-Cappellesso S. Gomez M. Ragea C. Sensebé L. (2008). Mesenchymal progenitor cells: tissue origin isolation and culture. Transfus. Med. Hemother. 35: 160-167.

  • Cui J.J. Chi Y. Du W.J. Yang S.G. Li X. Chen F. Ma F.X. Lu S.H. Han Z.C. (2013). Human umbilical cord mesenchymal stem cells reduce the sensitivity of HL-60 cells to cytarabine. Zhongguo Shi Yan Xue Ye Xue Za Zhi 21: 760-764.

  • Demazeau G. Rivalain N. (2011). High hydrostatic pressure and biology:abrief history. Appl. Microbiol. Biotechnol. 89: 1305-1314.

  • Dinnyes A. Polgar Z. Pribenszky C. Pirity M.K. (2010). Improved embryoid body cryopreservation and cardiomyocyte differentiation following high hydrostatic pressure treatment. Proc. The 1st International Congress on Controversies in Cryopreservation of Stem Cells Reproductive Cells Tissue and Organs Valencia Spain (Comet Med Israel) A-7.

  • Duszewska A.M. Reklewski Z. Pieńkowski M. Karasiewicz J. Modliński J.A. (2000). Development of bovine embryos on Vero/BRLcell monolayers (mixed co-culture). Theriogenology 4: 1239-1247.

  • Duszewska A.M. Wojdan J. Gawron W. Wenta- Muchalska E. Waś B. Wi- śniewska A. Reklewski Z. (2007). The development potential of bovine embryo co-culture with Vero and Vero/BRLcells. J. Anim. Feed Sci. 16: 370-379.

  • Emore S. (2007). Apoptosis:areview of programmed cel death. Toxicol. Pathol. 35: 495-516.

  • Fu X. He Y. Xie C. Liu W. (2008). Bone marrow mesenchymal stem cell transplantation improves ovarian function and structure in rats with chemotherapy-induced ovarian damage. Cytotherapy 10: 353-363.

  • Gala K. Burdzińska A. Pączek L. (2009). Bone marrow derived mesenchymal stem cells and aging (in Polish). Post. Biol. Kom. 37: 89-106.

  • Hajian M. Hosseini S.M. Asgari V. Ostadhoosseini S. Forouzanfar M. Nasr Esfahani M.H. (2011). Effect of culture system on developmental competence cryosurvival and DNA-fragmentation of in vitro bovine blastocysts. Int. J. Fertil. Steril. 5: 21-26.

  • Hay- Koren A. Bialik S. Levin- Salomon V. Kimchi A. (2017). Changes in c IAP2 survivin and Bim ELexpression characterize the swich from autophagy to apoptosis in prolonged starvation. J. Inter. Med. 281: 458-470.

  • Jeon K. Kim E.Y. Tae J.C. Lee C.H. Lee K.S. Kim Y.O. Jeong D.K. Cho S.K. Kim J.H. Lee H.Y. Riu K.Z. Cho S.G. Park S.P. (2008). Survivin protein expression in bovine follicular oocytes and their in vitro developmental competence. Anim. Reprod. Sci. 108: 319-333.

  • Jiang Z. Harrington P. Zhang M. Marjani S.L. Park J. Kuo L. Pribenszky C. Tian X.C. (2016). Effects of high hydrostatic pressure on expression profiles of in vitro produced vitrified bovine blastocysts. Sci. Rep. 6:21215; doi:

    • Crossref
    • Export Citation
  • Kątska L. Ryńska B. Smorąg Z. (1995). The effect of co-culture system on developmental capacity of bovine IVM/IVFoocytes. Theriogenology 43: 859-870.

  • Kątska-Książkiewicz L. Opiela J. Ryńska B. (2007). Effects of oocyte quality semen donor and embryo co-culture system on the efficiency of blastocyst production in goats. Theriogenology 68: 736-744.

  • Larsen B.D. Rampalli S. Burns L.E. Brunette S. Dilworth F.J. Megeney L.A. (2010). Caspase 3/caspase-activated DNase promote cell differentiation by inducing DNAstrand breaks. Proc. Natl. Acad. Sci. USA 107: 4230-4235.

  • Lee K.S. Santagostino S.F. Li D. Ramjit A. Serrano K. Ginsberg M.D. Ding B.S. Rafii S. Madoff D.C. (2017). Catheter-directed intraportal delivery of endothelial cell therapy for liver regeneration:afeasibility study inalarge-animal model of cirrhosis. Radiology doi:

    • Crossref
    • Export Citation
  • Lindenboim L. Yuan J. Stein R. (2000). Bclx Sand Bax induce different apoptotic pathways in PC12 cells. Oncogene 19: 1783-1793.

  • Ling B. Feng D.Q. Zhou Y. Gao T. Wei H.M. Tian Z.G. (2008). Effect of conditioned medium of mesenchymal stem cells on the in vitro maturation and subsequent development of mouse oocyte. Braz. J. Med. Biol. Res. 41: 978-985.

  • Liu X. Zou H. Slaughter C. Wang X. (1997). DFFaheterodimeric protein that functions downstream of caspase-3 to trigger DNAfragmentation during apoptosis. Cell 89: 175-184.

  • Maeda J. Kotsuji F. Negami A. Kamitani N. Tominaga T. (1996). In vitro development of bovine embryos in conditioned media from bovine granulosa cells and vero cells cultured in exogenous protein- and amino acid-free chemically defined human tubal fluid medium. Biol. Reprod. 54: 930-936.

  • Malina H.Z. Hess O.M. (2004). Xanthurenic acid translocates proapoptotic Bcl-2 family proteins into mitochondria and imparis mitochondrial function. BMC Cell Biol. 5: 14.

  • Mao F. Tu Q. Wang L. Chu F. Li X. Li H.S. Xu W. (2017). Mesenchymal stem cells and their therapeutic applications in inflammatory bowel disease. Oncotarget doi:

    • Crossref
    • Export Citation
  • Najar M. Raicevic G. Id Boufker H. Stamatopoulos B. De Bruyn C. Meule- man N. Bron D. Toungouz M. Lagneaux L. (2010). Modulated expression of adhesion molecules and galectin-1: role during mesenchymal stromal cell immunoregulatory functions. Exp. Hematol. 38: 922-932.

  • Opiela J. Samiec M. (2013). Characterization of mesenchymal stem cells and their application in experimental embryology. Pol. J. Vet. Sci. 16: 593-599.

  • Opiela J. Bülbül B. Romanek J. (2018). Negative results of using MSCfor bovine embryo development in different culture systems. Anim. Biotechnol. (in press).

  • Park H.Y. Kim E.Y. Lee S.E. Choi H.Y. Moon J.J. Park M.J. Son Y.J. Lee J.B. Jeong C.J. Lee D.S. Riu K.J. Park S.P. (2013) Effect of human adipose tissue-derived mesenchymal-stem-cell bioactive materials on porcine embryo development. Mol. Reprod. Dev. 80: 1035-1047.

  • Potapova I.A. Gaudette G.R. Brink P.R. Robinson R.B. Rosen M.R. Cohen I.S. Doronin S.V. (2007). Mesenchymal stem cells support migration extracellular matrix invasion proliferation and survival of endothelial cells in vitro. Stem Cells 25: 1761-1768.

  • Pribenszky C. Vajta G. Molna’r M. Du Y. Lin L. Bolund L. Yovich J. (2010). Stress for stress tolerance? Afundamentally new approach in mammalian embryology. Biol. Reprod. 83: 690-697.

  • Pribenszky C. Horváth A. Végh L. Huang S.Y. Kuo Y.H. Szenci O. (2011). Stress preconditioning of boar spermatozoa:anew approach to enhance semen quality. Reprod. Domest. Anim. 46 Suppl. 2: 26-30.

  • Rief S. Sinowatz F. Stojkovic M. Einspanier R. Wolf E. Prelle K. (2002). Effects ofanovel co-culture system on development metabolism and gene expression of bovine embryos produced in vitro. Reproduction 124: 543-556.

  • Rohban R. Pieber T.R. (2017). Mesenchymal stem and progenitor cells in regeneration: tissue specificity and regenerative potential. Stem Cells Int. doi:

    • Crossref
    • Export Citation
  • Romanek J. Opiela J. Lipiński D. Smorąg Z. (2017). The effect of high hydrostatic pressure on survival rate and quality of porcine Mesenchymal Stem Cells after cryopreservation. Anim. Biotechnol. 16: 1-10.

  • Safshekan F. Tafazzoli- Shadpour M. Shokrgozar M.A. Haghighipour N. Mahdian R. Hemmati A. (2012). Intermittent hydrostatic pressure enhances growth factorinduced chondroinduction of human adipose-derived mesenchymal stem cells. Artif. Organs. 36: 1065-1071.

  • Samiec M. Opiela J. Lipiński D. Romanek J. (2015). Trichostatin A-mediated epigenetic transformation of adult bone marrow-derived mesenchymal stem cells biases the in vitro developmental capability quality and pluripotency extent of porcine cloned embryos. Biomed. Res. Int. Article ID 814686 13 pages.

  • Son T.W. Yun S.P. Yong M.S. Seo B.N. Ryu J.M. Youn H.Y. Oh Y.M. Han H.J. (2013). Netrin-1 protects hypoxia-induced mitochondrial apoptosis through HSP27 expression via DCCand integrinα6β4-dependent Akt GSK-3β and HSF-1 in mesenchymal stem cells. Cell Death Dis. 4: 563-563.

  • Stachowiak M. Szczerbal I. Switonski M. (2016). Genetics of adiposity in large animal models for human obesity-studies on pigs and dogs. Prog. Mol. Biol. Transl. Sci. 140: 233-270.

  • Wang Q. Leader A. Tsang B.K. (2013). Follicular stage-dependent regulation of apoptosis and seroidogenesis by prohibitin in rat granulose cells. J. Ovarian. Res. 6: 23.

  • Warzych E. Pers- Kamczyc E. Krzywak A. Dudzińska S. Lechniak D. (2013). Apoptotic index within cumulus cells isaquestionable marker of meiotic competence of bovine ooctes matured in vitro. Reprod. Biol. 13: 82-87.

  • Wolff H.S. Fredrickson J.R. Walker D.L. Morbeck D.E. (2013). Advances in quality control: mouse embryo morphokinetics are sensitive markers of in vitro stress. Hum. Reprod. 28: 1776-1782.

  • Zeyland J. Woźniak A. Gawrońska B. Juzwa W. Jura J. Nowak A. Słom - ski R. Smorąg Z. Szalata M. Mazurek U. Lipiński D. (2014). Double transgenic pigs with combined expression of humanα12-fucosyltransferase andα-galactosidase designed to avoid hyperacute xenograft rejection. Arch. Immunol. Ther. Exp. (Warsz). 62: 411-422.

  • Zhang L. Weston A.M. Denniston R.S. Goodeaux L.L. Godke R.A. Wolf D.P. (1994). Developmental potential of rhesus monkey embryos produced by in vitro fertilization. Biol. Reprod. 51: 433-440.

Search
Journal information
Impact Factor

IMPACT FACTOR 2018: 1.515
5-year IMPACT FACTOR: 1.246

CiteScore 2018: 1.4

SCImago Journal Rank (SJR) 2018: 0.509
Source Normalized Impact per Paper (SNIP) 2018: 0.869

Metrics
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 466 259 8
PDF Downloads 225 127 6