Homing and Restorative Effects of Bone Marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats

Molecules and Cells

Volumn 37, Issue 12, 2015, Pages 865-872

  Liu, Jiabin ^a,b   Zhang, Haiying ^a   Zhang, Yun ^b   Li, Nan ^b   Wen, Yuku ^b   Cao, Fanglei ^b   Ai, Hao ^a,b   Xue, Xiaoou ^c  

^a JINZHOU MEDICAL UNIVERSITY   (China)

^b Medical University   (China)

^c BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Bone marrow derived mesenchymal stem cells; Cisplatin; Homing; Intravenous injection; Premature ovarian failure

Indexed keywords

CISPLATIN; ENHANCED GREEN FLUORESCENT PROTEIN; ESTRADIOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL HOMING; CELL LABELING; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; FEMALE; GRANULOSA CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OVARY FUNCTION; PREMATURE OVARIAN FAILURE; RAT; ANIMAL; ANTIBODY SPECIFICITY; BONE MARROW TRANSPLANTATION; CELL CULTURE; CELL MOTION; CHEMICALLY INDUCED; HUMAN; INTRAPERITONEAL DRUG ADMINISTRATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRIMARY OVARIAN INSUFFICIENCY; PROCEDURES; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; BONE MARROW TRANSPLANTATION; CELL MOVEMENT; CELLS, CULTURED; CISPLATIN; FEMALE; GRANULOSA CELLS; HUMANS; INJECTIONS, INTRAPERITONEAL; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; ORGAN SPECIFICITY; PRIMARY OVARIAN INSUFFICIENCY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84939942485     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2014.0145     Document Type: Article

References (44)

1. Abd-Allah, S.H., Shalaby, S.M., Pasha, H.F., El-Shal, A.S., Raafat, N., Shabrawy, S.M., Awad, H.A., Amer, M.G., Gharib, M.A., El Gendy, E.A., et al. (2013). Mechanistic action of mesenchymal stem cell injection in the treatment of chemically induced ovarian failure in rabbits. Cytotherapy 15, 64-75.
2. Agung, M., Ochi, M., Yanada, S., Adachi, N., Izuta, Y., Yamasaki, T., and Toda, K. (2006). Mobilization of bone marrow-derived mesenchymal stem cells into the injured tissues after intraarticular injection and their contribution to tissue regeneration. Knee Surg. Sports Traumatol. Arthrosc. 14, 1307-1314.
3. Ai, H., Zhang, H., Zhang, Y., and Liu, Y. (2012). Mouse ovarian- related gene expression profiles change with intraperitoneal injection of cisplatin. African J. Pharm. Pharm. 6, 2119-2122.
4. Antoine, C., Ameye, L., Paesmans, M., and Rozenberg, S. (2013). Systematic review about breast cancer incidence in relation to hormone replacement therapy use. Climacteric 17, 116-135.
5. Bi, B., Schmitt, R., Israilova, M., Nishio, H., and Cantley, L.G. (2007). Stromal cells protect against acute tubular injury via an endocrine effect. J. Am. Soc. Nephrol.18, 2486-2496.
6. Bosch, P., Fouletier-Dilling, C., Olmsted-Davis, E., Davis, A., and Stice, S. (2006). Efficient adenoviral-mediated gene delivery into porcine mesenchymal stem cells. Mol. Reprod. Dev. 73, 1393-1403.
7. Das, B., Antoon, R., Tsuchida, R., Lotfi, S., Morozova, O., Farhat, W., Malkin, D., Koren, G., Yeger, H., and Baruchel, S. (2008). Squalene selectively protects mouse bone marrow progenitors against cisplatin and carboplatin-induced cytotoxicity in vivo without protecting tumor growth. Neoplasia 10, 1105-1119.
8. De Vos, F., Nuver, J., Willemse, P., van der Zee, A., Messerschmidt, J., Burgerhof, J., De Vries, E., and Gietema, J. (2004). Longterm survivors of ovarian malignancies after cisplatin-based chemotherapy: cardiovascular risk factors and signs of vascular damage. Eur. J. Cancer 40, 696-700.
9. Donnez, J., and Dolmans, M.-M. (2013). Fertility preservation in women. Nat. Rev. Endocrinol. 9, 735-749.
10. Forte, G., Minieri, M., Cossa, P., Antenucci, D., Sala, M., Gnocchi, V., Fiaccavento, R., Carotenuto, F., DeVito, P., Baldini, P.M., et al. (2006). Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 24, 23-33.
11. Frenette, P.S., Pinho, S., Lucas, D., and Scheiermann, C. (2013). Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Ann. Rev. Immunol. 31, 285-316.
12. Fu, X., He, Y., Xie, C., and 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.
13. Ghadami, M., El-Demerdash, E., Zhang, D., Salama, S.A., Binhazim, A.A., Archibong, A.E., Chen, X., Ballard, B.R., Sairam, M.R., and Al-Hendy, A. (2012). Bone marrow transplantation restores follicular maturation and steroid hormones production in a mouse model for primary ovarian failure. PLoS One 7, e32462.
14. Guo, J.Q., Gao, X., Lin, Z.J., Wu, W.Z., Huang, L.H., Dong, H.Y., Chen, J., Lu, J., Fu, Y.F., Wang, J., et al. (2013). BMSCs reduce rat granulosa cell apoptosis induced by cisplatin and perimenopause. BMC Cell Biol. 14, 1-9.
15. Iorio, R., Castellucci, A., Ventriglia, G., Teoli, F., Cellini, V., Macchiarelli, G., and Cecconi, S. (2014). Ovarian toxicity: from environmental exposure to chemotherapy. Curr. Pharm. Des. 20, 5388-5397.
16. Johnson, J., Bagley, J., Skaznik-Wikiel, M., Lee, H.-J., Adams, G.B., Niikura, Y., Tschudy, K.S., Tilly, J.C., Cortes, M.L., Forkert, R., et al. (2005). Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 122, 303-315.
17. Kilic, S., Pinarli, F., Ozogul, C., Tasdemir, N., Naz Sarac, G., and Delibasi, T. (2013). Protection from cyclophosphamide-induced ovarian damage with bone marrow-derived mesenchymal stem cells during puberty. Gynecol. Endocrinol. 30, 135-140.
18. Kupcova Skalnikova, H. (2013). Proteomic techniques for characterization of mesenchymal stem cell secretome. Biochimie 95, 2196-2211.
19. Lai, D., Wang, F., Chen, Y., Wang, L., Wang, Y., and Cheng, W. (2013). Human amniotic fluid stem cells have a potential to recover ovarian function in mice with chemotherapy-induced sterility. BMC Dev. Biol. 13, 34.
20. Lana, M.B.P., Straminsky, V., Onetto, C., Amuchastegui, J.M., Blanco, G., Galluzzo, L., Provenzano, S., and Nolting, M. (2010). What is really responsible for bone loss in spontaneous premature ovarian failure? A new enigma. Gynecol. Endocrinol. 26, 755-759.
21. Lee, O., Coathup, M., Goodship, A., and Blunn, G. (2005). Use of mesenchymal stem cells to facilitate bone regeneration in normal and chemotherapy-treated rats. Tissue Eng. 11, 1727- 1735.
22. Lee, H.-J., Selesniemi, K., Niikura, Y., Niikura, T., Klein, R., Dombkowski, D.M., and Tilly, J.L. (2007). 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. 25, 3198-3204.
23. Liu, T., Huang, Y., Guo, L., Cheng, W., and Zou, G. (2012). CD44+/ CD105+ human amniotic fluid mesenchymal stem cells survive and proliferate in the ovary long-term in a mouse model of chemotherapy-induced premature ovarian failure. Int. J. Med Sci. 9, 592-602.
24. Lue, Y., Erkkila, K., Liu, P.Y., Ma, K., Wang, C., Hikim, A.S., and Swerdloff, R.S. (2007). Fate of bone marrow stem cells transplanted into the testis: potential implication for men with testicular failure. Am. J. Pathol. 170, 899-908.
25. Mörse, H., Elfving, M., Lindgren, A., Wölner-Hanssen, P., Andersen, C.Y., and Øra, I. (2013). Acute onset of ovarian dysfunction in young females after start of cancer treatment. Pediatr. Blood Cancer 60, 676-681.
26. Maclaran, K., and Panay, N. (2011). Premature ovarian failure. J. Fam. Plann. Reprod. Health Care 37, 35-42.
27. Maruo, T., Laoag-Fernandez, J., Takekida, S., Peng, X., Deguchi, J., Samoto, T., Kondo, H., and Matsuo, H. (1999). Regulation of granulosa cell proliferation and apoptosis during follicular development. Gynecol. Endocrinol. 13, 410-419.
28. Matsuda, F., Inoue, N., Manabe, N., and Ohkura, S. (2011). Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J. Reprod. Dev. 58, 44-50.
29. Miyamoto, Y., Shimada, K., Sakaguchi, Y., and Miyamoto, M. (2007). Cisplatin (CDDP)-induced acute toxicity in an experimental model of hepatic fibrosis. J. Toxicol. Sci. 32, 311-319.
30. Muscari, C., Bonafè, F., Martin-Suarez, S., Valgimigli, S., Valente, S., Fiumana, E., Fiorelli, F., Rubini, G., Guarnieri, C., Caldarera, C.M., et al. (2013). Restored perfusion and reduced inflammation in the infarcted heart after grafting stem cells with a hyaluronan-based scaffold. J. Cell. Mol. Med. 17, 518-530.
31. Nayernia, K., Lee, J.H., Drusenheimer, N., Nolte, J., Wulf, G., Dressel, R., Gromoll, J., and Engel, W. (2006). Derivation of male germ cells from bone marrow stem cells. Lab. Invest. 86, 654-663
32. Nozaki, Y., Furubo, E., Matsuno, T., Fukui, R., Kizawa, K., Kozaki, T., and Sanzen, T. (2009). Collaborative work on evaluation of ovarian toxicity 6. Two-or four-week repeated-dose studies and fertility study of cisplatin in female rats. J. Toxicol. Sci. 34, SP73-81.
33. Ohishi, M., and Schipani, E. (2010). Bone marrow mesenchymal stem cells. J. Cell. Biochem. 109, 277-282.
34. Rüster, B., Grace, B., Seitz, O., Seifried, E., and Henschler, R. (2005). Induction and detection of human mesenchymal stem cell migration in the 48-well reusable transwell assay. Stem Cells Dev. 14, 231-235.
35. Santos, N., Catao, C., Martins, N., Curti, C., Bianchi, M., and Santos, A. (2007). Cisplatin-induced nephrotoxicity is associated with oxidative stress, redox state unbalance, impairment of energetic metabolism and apoptosis in rat kidney mitochondria. Arch. Toxicol. 81, 495-504.
36. Schmidt, A., Ladage, D., Schinköthe, T., Klausmann, U., Ulrichs, C., Klinz, F.J., Brixius, K., Arnhold, S., Desai, B., and Mehlhorn, U. (2006). Basic fibroblast growth factor controls migration in human mesenchymal stem cells. Stem Cells 24, 1750-1758.
37. Selesniemi, K., Lee, H.-J., Niikura, T., and Tilly, J.L. (2009). Young adult donor bone marrow infusions into female mice postpone age-related reproductive failure and improve offspring survival. Aging 1, 49-57.
38. Siddik, Z.H. (2003). Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 22, 7265-7279.
39. Sohni, A., and Verfaillie, C.M. (2013). Mesenchymal stem cells migration homing and tracking. Stem Cells Int. 2013, 130763.
40. Takehara, Y., Yabuuchi, A., Ezoe, K., Kuroda, T., Yamadera, R., Sano, C., Murata, N., Aida, T., Nakama, K., Aono, F., et al. (2013). The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function. Lab. Invest. 93, 181-193.
41. Tannock, I.F., Ahles, T.A., Ganz, P.A., and van Dam, F.S. (2004). Cognitive impairment associated with chemotherapy for cancer: report of a workshop. J. Clin. Oncol. 22, 2233-2239.
42. Wang, S., Yu, L., Sun, M., Mu, S., Wang, C., Wang, D., and Yao, Y. (2013). The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure. Biomed Res. Int. 2013, 690491.
43. Yuan, L., Wu, M.J., Sun, H.Y., Xiong, J., Zhang, Y., Liu, C.Y., Fu, L.L., Liu, D.M., Liu, H.-Q., and Mei, C.-L. (2011). VEGF-modified human embryonic mesenchymal stem cell implantation enhances protection against cisplatin-induced acute kidney injury. Am. J. Physiol. Renal. Physiol. 300, F207-F218.
44. Zhang, A., Wang, Y., Ye, Z., Xie, H., Zhou, L., and Zheng, S. (2010). Mechanism of TNF- -nduced migration and hepatocyte growth factor production in human mesenchymal stem cells. J. Cell. Biochem. 111, 469-475.