Download fulltext
HTML
Adib, M., Morteza Seifati, S., Dehghani Ashkezari, M., Khoradmehr, A., Rezaee-Ranjbar-Sardari, R., Sadat Tahajjodi, S., & Aflatoonian, B. (2020). The effect of the human cumulus cells-conditioned medium on in vitro maturation of mouse oocyte: An experimental study. International Journal of Reproductive BioMedicine (IJRM), 18(12), 1019–1028. https://doi.org/10.18502/ijrm.v18i12.8023
https://doi.org/10.18502/ijrm.v18i12.8023
statistics
- 357 Abstract Views
- 138 PDF Views
- 0 HTML Views
- Cited by 3 articles
authors
-
Maryam Adib
Maryam Adib
Medical Biotechnology Research Center, Ashkezar Branch, Islamic Azad University, Ashkezar, Yazd, Iran
-
Seyed Morteza Seifati
Seyed Morteza Seifati
Medical Biotechnology Research Center, Ashkezar Branch, Islamic Azad University, Ashkezar, Yazd, Iran
-
Mahmood Dehghani Ashkezari
Mahmood Dehghani Ashkezari
Medical Biotechnology Research Center, Ashkezar Branch, Islamic Azad University, Ashkezar, Yazd, Iran
-
Arezoo Khoradmehr
Arezoo Khoradmehr
Stem Cell Biology Research Center, Yazd Reproductive Sciences Institute, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
-
Roshan Rezaee-Ranjbar-Sardari
Roshan Rezaee-Ranjbar-Sardari
Medical Biotechnology Research Center, Ashkezar Branch, Islamic Azad University, Ashkezar, Yazd, Iran
-
Somayyeh Sadat Tahajjodi
Somayyeh Sadat Tahajjodi
Stem Cell Biology Research Center, Yazd Reproductive Sciences Institute, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
-
Behrouz Aflatoonian
Behrouz Aflatoonian
Stem Cell Biology Research Center, Yazd Reproductive Sciences Institute, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Published Date
- Dec 21, 2020
The effect of the human cumulus cells-conditioned medium on in vitro maturation of mouse oocyte: An experimental study
Abstract
Background: To increase the results of infertility treatment, many efforts have been made to improve the treatment methods. As assisted reproductive technology is mainly using cell culture methods, one of the approaches to improve this technology is conditioned medium from different sources. It is desirable to apply in vitro maturation (IVM) and use oocytes from normal cycles instead of stimulating ovulation.
Objective: To investigate the effect of human cumulus cell condition medium (hCCCM) on the IVM of immature mouse oocytes and morphology.
Materials and Methods: In this experimental study, 240 germinal vesile oocytes were collected from four-six wk-old mice after 48 hr of 5IU pregnant mare serum gonadotropin (PMSG) injection and cultured in hCCCM (test group, n = 120) and DMEM + 20% FBS (control group, n = 120). The IVM rates and changes in perivitelline space (PVS) and shape were investigated at 8, 16, and 24 hr following the culture. The mature (MII) oocytes were subjected to in vitro fertilization (IVF) and the fertilization rate was assessed in three days.
Results: A significant difference was observed between the maturation rates in the hCCCM and control groups (24.16% vs 0%; p = 0.001), as well as morphologic changes between the two groups (p = 0.04, p = 0.05). The development rate for MII oocytes attained from IVM in the hCCCM group was 27.58% (2-cell) and 6.89% (4-cell). Data displayed that hCCCM is an effective medium for oocytes maturation compared to the control medium.
Conclusion: hCCCM supports oocyte in vitro growth and maturation. Moreover, hCCCM changes the oocyte shape and size of perivitelline space.
Key words: Germinal vesicle, Cumulus cell, Conditioned medium, In vitro fertilization, In vitro maturation, Oocyte.
References
[1] Hoseini FS, Mugahi SMHN, Akbari-Asbagh F, Eftekhari-Yazdi P, Aflatoonian B, Aghaee-Bakhtiari SH, et al. A randomized controlled trial of gonadotropin-releasing hormone agonist versus gonadotropin-releasing hormone antagonist in Iranian infertile couples: oocyte gene expression. Daru 2014; 22: 67–75.
[2] Abbara A, Clarke SA, Dhillo WS. Novel concepts for inducing final oocyte maturation in in vitro fertilization treatment. Endocr Rev 2018; 39: 593– 628.
[3] Yang ZY, Chian RC. Development of in vitro maturation techniques for clinical applications. Fertil Steril 2017; 108: 577–584.
[4] Walls ML, Hart RJ. In vitro maturation. Best Pract Res Clin Obstet Gynaecol 2018; 53: 60–72.
[5] Lonergan P, Fair T. Maturation of oocytes in vitro. Annu Rev Anim Biosci 2016; 4: 255–268.
[6] Child TJ, Abdul-Jalil AK, Gulekli B, Tan SL. In vitro maturation and fertilization of oocytes from unstimulated normal ovaries, polycystic ovaries, and women with polycystic ovary syndrome. Fertil Steril 2001; 76: 936–942.
[7] Rezaee-Ranjbar-Sardari R, Khoradmehr A, Mazaheri F, Tahajjodi SS, Aflatoonian B. An investigation of the effect of the human cumulus cell conditioned medium on mouse oocytes in vitro maturation. Int J Reprod BioMed 2019; 17 (Suppl.): 106–107.
[8] Uhde K, van Tol HT, Stout TA, Roelen BA. Metabolomic profiles of bovine cumulus cells and cumulus-oocyte-complex-conditioned medium during maturation in vitro. Sci Rep 2018; 8: 9477– 9490.
[9] Abdel-Ghani MA, Abe Y, Asano T, Hamano S, Suzuki H. Effect of bovine cumulus-oocyte complexesconditioned medium on in-vitro maturation of canine oocytes. Reprod Med Biol 2011; 10: 43–49.
[10] Fatehi A, Zeinstra E, Kooij R, Colenbrander B, Bevers M. Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 2002; 57: 1347–1355.
[11] Shah SM, Saini N, Ashraf S, Singh MK, Manik RS, Singla SK, et al. Cumulus cell-conditioned medium supports embryonic stem cell differentiation to germ cell-like cells. Reprod Fertil Dev 2017; 29: 679–693.
[12] Tahajjodi SS, Aflatoonian R, Agharahimi A, Hajizadeh-Tafti F, Akyash F, et al. Cumulus cells conditioned medium as an in vitro niche for differentiation of human embryonic stem cells to female germ cells. Hum Reprod 2019; 34: 793.
[13] Mirzaeian L, Eftekhari-Yazdi P, Esfandiari F, Eivazkhani F, Rezazadeh Valojerdi M, Moini A, et al. Induction of mouse peritoneum mesenchymal stem cells into germ cell-like cells using follicular fluid and cumulus cells-conditioned media. Stem Cells Dev 2019; 28: 554–564.
[14] Atrabi MJ, Akbarinejad V, Khanbabaee R, Dalman A, Amorim CA, Najar−Asl M, et al. Formation and activation induction of primordial follicles using granulosa and cumulus cells conditioned media. J Cell Physiol 2019; 234: 10148–10156.
[15] Tahajjodi SS, Farashahi Yazd E, Agha-Rahimi A, Aflatoonian R, Khalili MA, Mohammadi M, et al. Biological and physiological characteristics of human cumulus cells in adherent culture condition. Int J Reprod BioMed 2020; 18: 1–10.
[16] Adib M, Seifati SM, Dehghani Ashkezari M, Akyash F, Khoradmehr A, Aflatoonian B. Effect of human testicular cells conditioned medium on in vitro maturation and morphology of mouse oocytes. Int J Fertil Steril 2020; 14: 176–184.
[17] Allahveisi A, Yousefian E, Rezaie M, Nikkhoo B. Comparison of morphometric and morphology oocytes after in vitro maturation between healthy women and patients with polycystic ovarian syndrome. Acta Endocrinol 2019; 15: 295–300.
[18] Chang EM, Song HS, Lee DR, Lee WS, Yoon TK. In vitro maturation of human oocytes: its role in infertility treatment and new possibilities. Clin Exp Reprod Med 2014; 41: 41–46.
[19] Coticchio G, Dal-Canto M, Guglielmo MC, Mignini- Renzini M, Fadini R. Human oocyte maturation in vitro. Int J Dev Biol 2012; 56: 909–918.
[20] Yeo CX, Gilchrist RB, Thompson JG, Lane M. Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum Reprod 2008; 23: 67–73.
[21] Sutton-McDowall ML, Mottershead DG, Gardner DK, Gilchrist RB, Thompson JG. Metabolic differences in bovine cumulus-oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15. Biol Reprod 2012; 87: 1–8.
[22] Coticchio G, Dal Canto M, Mignini Renzini M, Guglielmo MC, Brambillasca F, Turchi D, et al. Oocyte maturation: gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum Reprod Update 2015; 21: 427–454.
[23] Richani D, Gilchrist RB. The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update 2018; 24: 1–14.
[24] Sato A, Sarentonglaga B, Ogata K, Yamaguchi M, Hara A, Atchalalt K, et al. Effects of insulin-like growth factor-1 on the in vitro maturation of canine oocytes. J Reprod Dev 2018; 64: 83–88.
[25] Pereira LMC, Bersano PRO, Rocha DD, Lopes MD. Effect of EGF on expression and localization of maturation−promoting factor, mitogen−activated protein kinase, p34cdc2 and cyclin B during different culture periods on in vitro maturation of canine oocytes. Reprod Domest Anim 2019; 54: 325–341.
[26] Abkenar ZO, Ganji R, Khajehrahimi AE, Bahadori MH. Vitrification and subsequent in vitro maturation of mouse preantral follicles in presence of growth factors. Cell J 2014; 16: 271–278.
[27] Ben-Ami I, Komsky A, Bern O, Kasterstein E, Komarovsky D, Ron-El R. In vitro maturation of human germinal vesicle-stage oocytes: role of epidermal growth factor-like growth factors in the culture medium. Hum Reprod 2011; 26: 76–81.
[28] Su J, Hu G, Wang Y, Liang D, Gao M, Sun H, et al. Recombinant human growth differentiation factor- 9 improves oocyte reprogramming competence and subsequent development of bovine cloned embryos. Cell Reprogram 2014; 16: 281–289.
[29] Cook-Andersen H, Curnow KJ, Su HI, Chang RJ, Shimasaki S. Growth and differentiation factor 9 promotes oocyte growth at the primary but not the early secondary stage in three-dimensional follicle culture. J Assist Reprod Genet 2016; 33: 1067–1077.
[30] Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJ, Hovatta O. Growth differentiation factor- 9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J Clin Endocrinol Metab 2002; 87: 316–321.
[31] Zand E, Fathi R, Nasrabadi MH, Atrabi MJ, Spears N, Akbarinejad V. Maturational gene upregulation and mitochondrial activity enhancement in mouse in vitro matured oocytes and using granulosa cell conditioned medium. Zygote 2018; 26: 366–371.
[32] Lee SR, Kim MO, Kim SH, Kim BS, Yoo DH, Park YS, et al. Effect of conditioned medium of mouse embryonic fibroblasts produced from ECSOD transgenic mice in nuclear maturation of canine oocytes in vitro. Anim Reprod Sci 2007; 99: 106– 116.
[33] Jafarzadeh H, Nazarian H, Ghaffari Novin M, Shams Mofarahe Z, Eini F, Piryaei A. Improvement of oocyte in vitro maturation from mice with polycystic ovary syndrome by human mesenchymal stromal cellconditioned media. J Cell Biochem 2018; 119: 10365– 10375.
[34] Sacha C, Kaser D, Farland L, Srouji S, Missmer S, Racowsky C. The effect of short-term exposure of cumulus-oocyte complexes to in vitro maturation medium on yield of mature oocytes and usable embryos in stimulated cycles. J Assist Reprod Genet 2018; 35: 841–849.
[35] Bernal Ulloa SM, Heinzmann J, Herrmann D, Timmermann B, Baulain U, Großfeld R, et al. Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote 2015; 23: 367–377.
[36] Mikkelsen AL, Lindenberg S. Morphology of in-vitro matured oocytes: impact on fertility potential and embryo quality. Hum Reprod 2001; 16: 1714–1718.
[37] Hassa H, Aydın Y, Taplamacıoğlu F. The role of perivitelline space abnormalities of oocytes in the developmental potential of embryos. J Turk Ger Gynecol Assoc 2014; 15: 161–163.
[2] Abbara A, Clarke SA, Dhillo WS. Novel concepts for inducing final oocyte maturation in in vitro fertilization treatment. Endocr Rev 2018; 39: 593– 628.
[3] Yang ZY, Chian RC. Development of in vitro maturation techniques for clinical applications. Fertil Steril 2017; 108: 577–584.
[4] Walls ML, Hart RJ. In vitro maturation. Best Pract Res Clin Obstet Gynaecol 2018; 53: 60–72.
[5] Lonergan P, Fair T. Maturation of oocytes in vitro. Annu Rev Anim Biosci 2016; 4: 255–268.
[6] Child TJ, Abdul-Jalil AK, Gulekli B, Tan SL. In vitro maturation and fertilization of oocytes from unstimulated normal ovaries, polycystic ovaries, and women with polycystic ovary syndrome. Fertil Steril 2001; 76: 936–942.
[7] Rezaee-Ranjbar-Sardari R, Khoradmehr A, Mazaheri F, Tahajjodi SS, Aflatoonian B. An investigation of the effect of the human cumulus cell conditioned medium on mouse oocytes in vitro maturation. Int J Reprod BioMed 2019; 17 (Suppl.): 106–107.
[8] Uhde K, van Tol HT, Stout TA, Roelen BA. Metabolomic profiles of bovine cumulus cells and cumulus-oocyte-complex-conditioned medium during maturation in vitro. Sci Rep 2018; 8: 9477– 9490.
[9] Abdel-Ghani MA, Abe Y, Asano T, Hamano S, Suzuki H. Effect of bovine cumulus-oocyte complexesconditioned medium on in-vitro maturation of canine oocytes. Reprod Med Biol 2011; 10: 43–49.
[10] Fatehi A, Zeinstra E, Kooij R, Colenbrander B, Bevers M. Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 2002; 57: 1347–1355.
[11] Shah SM, Saini N, Ashraf S, Singh MK, Manik RS, Singla SK, et al. Cumulus cell-conditioned medium supports embryonic stem cell differentiation to germ cell-like cells. Reprod Fertil Dev 2017; 29: 679–693.
[12] Tahajjodi SS, Aflatoonian R, Agharahimi A, Hajizadeh-Tafti F, Akyash F, et al. Cumulus cells conditioned medium as an in vitro niche for differentiation of human embryonic stem cells to female germ cells. Hum Reprod 2019; 34: 793.
[13] Mirzaeian L, Eftekhari-Yazdi P, Esfandiari F, Eivazkhani F, Rezazadeh Valojerdi M, Moini A, et al. Induction of mouse peritoneum mesenchymal stem cells into germ cell-like cells using follicular fluid and cumulus cells-conditioned media. Stem Cells Dev 2019; 28: 554–564.
[14] Atrabi MJ, Akbarinejad V, Khanbabaee R, Dalman A, Amorim CA, Najar−Asl M, et al. Formation and activation induction of primordial follicles using granulosa and cumulus cells conditioned media. J Cell Physiol 2019; 234: 10148–10156.
[15] Tahajjodi SS, Farashahi Yazd E, Agha-Rahimi A, Aflatoonian R, Khalili MA, Mohammadi M, et al. Biological and physiological characteristics of human cumulus cells in adherent culture condition. Int J Reprod BioMed 2020; 18: 1–10.
[16] Adib M, Seifati SM, Dehghani Ashkezari M, Akyash F, Khoradmehr A, Aflatoonian B. Effect of human testicular cells conditioned medium on in vitro maturation and morphology of mouse oocytes. Int J Fertil Steril 2020; 14: 176–184.
[17] Allahveisi A, Yousefian E, Rezaie M, Nikkhoo B. Comparison of morphometric and morphology oocytes after in vitro maturation between healthy women and patients with polycystic ovarian syndrome. Acta Endocrinol 2019; 15: 295–300.
[18] Chang EM, Song HS, Lee DR, Lee WS, Yoon TK. In vitro maturation of human oocytes: its role in infertility treatment and new possibilities. Clin Exp Reprod Med 2014; 41: 41–46.
[19] Coticchio G, Dal-Canto M, Guglielmo MC, Mignini- Renzini M, Fadini R. Human oocyte maturation in vitro. Int J Dev Biol 2012; 56: 909–918.
[20] Yeo CX, Gilchrist RB, Thompson JG, Lane M. Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum Reprod 2008; 23: 67–73.
[21] Sutton-McDowall ML, Mottershead DG, Gardner DK, Gilchrist RB, Thompson JG. Metabolic differences in bovine cumulus-oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15. Biol Reprod 2012; 87: 1–8.
[22] Coticchio G, Dal Canto M, Mignini Renzini M, Guglielmo MC, Brambillasca F, Turchi D, et al. Oocyte maturation: gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum Reprod Update 2015; 21: 427–454.
[23] Richani D, Gilchrist RB. The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update 2018; 24: 1–14.
[24] Sato A, Sarentonglaga B, Ogata K, Yamaguchi M, Hara A, Atchalalt K, et al. Effects of insulin-like growth factor-1 on the in vitro maturation of canine oocytes. J Reprod Dev 2018; 64: 83–88.
[25] Pereira LMC, Bersano PRO, Rocha DD, Lopes MD. Effect of EGF on expression and localization of maturation−promoting factor, mitogen−activated protein kinase, p34cdc2 and cyclin B during different culture periods on in vitro maturation of canine oocytes. Reprod Domest Anim 2019; 54: 325–341.
[26] Abkenar ZO, Ganji R, Khajehrahimi AE, Bahadori MH. Vitrification and subsequent in vitro maturation of mouse preantral follicles in presence of growth factors. Cell J 2014; 16: 271–278.
[27] Ben-Ami I, Komsky A, Bern O, Kasterstein E, Komarovsky D, Ron-El R. In vitro maturation of human germinal vesicle-stage oocytes: role of epidermal growth factor-like growth factors in the culture medium. Hum Reprod 2011; 26: 76–81.
[28] Su J, Hu G, Wang Y, Liang D, Gao M, Sun H, et al. Recombinant human growth differentiation factor- 9 improves oocyte reprogramming competence and subsequent development of bovine cloned embryos. Cell Reprogram 2014; 16: 281–289.
[29] Cook-Andersen H, Curnow KJ, Su HI, Chang RJ, Shimasaki S. Growth and differentiation factor 9 promotes oocyte growth at the primary but not the early secondary stage in three-dimensional follicle culture. J Assist Reprod Genet 2016; 33: 1067–1077.
[30] Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJ, Hovatta O. Growth differentiation factor- 9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J Clin Endocrinol Metab 2002; 87: 316–321.
[31] Zand E, Fathi R, Nasrabadi MH, Atrabi MJ, Spears N, Akbarinejad V. Maturational gene upregulation and mitochondrial activity enhancement in mouse in vitro matured oocytes and using granulosa cell conditioned medium. Zygote 2018; 26: 366–371.
[32] Lee SR, Kim MO, Kim SH, Kim BS, Yoo DH, Park YS, et al. Effect of conditioned medium of mouse embryonic fibroblasts produced from ECSOD transgenic mice in nuclear maturation of canine oocytes in vitro. Anim Reprod Sci 2007; 99: 106– 116.
[33] Jafarzadeh H, Nazarian H, Ghaffari Novin M, Shams Mofarahe Z, Eini F, Piryaei A. Improvement of oocyte in vitro maturation from mice with polycystic ovary syndrome by human mesenchymal stromal cellconditioned media. J Cell Biochem 2018; 119: 10365– 10375.
[34] Sacha C, Kaser D, Farland L, Srouji S, Missmer S, Racowsky C. The effect of short-term exposure of cumulus-oocyte complexes to in vitro maturation medium on yield of mature oocytes and usable embryos in stimulated cycles. J Assist Reprod Genet 2018; 35: 841–849.
[35] Bernal Ulloa SM, Heinzmann J, Herrmann D, Timmermann B, Baulain U, Großfeld R, et al. Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote 2015; 23: 367–377.
[36] Mikkelsen AL, Lindenberg S. Morphology of in-vitro matured oocytes: impact on fertility potential and embryo quality. Hum Reprod 2001; 16: 1714–1718.
[37] Hassa H, Aydın Y, Taplamacıoğlu F. The role of perivitelline space abnormalities of oocytes in the developmental potential of embryos. J Turk Ger Gynecol Assoc 2014; 15: 161–163.