The potentials of umbilical cord-derived mesenchymal stem cells in the treatment of multiple sclerosis

References

Aggarwal, S. and Pittenger, M.F. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815–1822.10.1182/blood-2004-04-1559Search in Google Scholar PubMed

Akimoto, K., Kimura, K., Nagano, M., Takano, S., To’a Salazar, G., Yamashita, T., and Ohneda, O. (2013). Umbilical cord blood-derived mesenchymal stem cells inhibit, but adipose tissue-derived mesenchymal stem cells promote, glioblastoma multiforme proliferation. Stem Cells Dev. 22, 1370–1386.10.1089/scd.2012.0486Search in Google Scholar PubMed PubMed Central

Al Jumah, M.A. and Abumaree, M.H. (2012). The immunomodulatory and neuroprotective effects of mesenchymal stem cells (MSCs) in experimental autoimmune encephalomyelitis (EAE): a model of multiple sclerosis (MS). Int. J. Mol. Sci. 13, 9298–9331.10.3390/ijms13079298Search in Google Scholar PubMed PubMed Central

Alemi Serej, F., Pourhassan-Moghaddam, M., Ebrahimi Kalan, M., Mehdipour, A., Aliyari Serej, Z., and Ebrahimi-Kalan, A. (2018). Targeting the PI3K/Akt/mTOR signaling pathway: applications of nanotechnology. Crescent J. Med. Biol. Sci. 5, 7–13.Search in Google Scholar

Aliyari, Z., Soleimanirad, S., Sayyah Melli, M., Tayefi Nasrabadi, H., and Nozad Charoudeh, H. (2015). IL2rg cytokines enhance umbilical cord blood CD34⁺ cells differentiation to T cells. Adv. Pharm. Bull. 5, 615–619.10.15171/apb.2015.083Search in Google Scholar PubMed PubMed Central

Alizadeh-Ghodsi, M., Zavvari, A., Ebrahimi-Kalan, A., Shiri-Shahsavar, M.R., and Yousefi, B. (2018). The hypothetical roles of arsenic in multiple sclerosis by induction of inflammation and aggregation of tau protein: a commentary. Nutr. Neurosci. 21, 92–96.10.1080/1028415X.2016.1239399Search in Google Scholar PubMed

Amariglio, N., Hirshberg, A., Scheithauer, B.W., Cohen, Y., Loewenthal, R., Trakhtenbrot, L., Paz, N., Koren-Michowitz, M., Waldman, D., Leider-Trejo, L., et al. (2009). Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med. 6, e1000029.10.1371/journal.pmed.1000029Search in Google Scholar PubMed PubMed Central

Amati, E., Sella, S., Perbellini, O., Alghisi, A., Bernardi, M., Chieregato, K., Lievore, C., Peserico, D., Rigno, M., Zilio, A., et al. (2017). Generation of mesenchymal stromal cells from cord blood: evaluation of in vitro quality parameters prior to clinical use. Stem Cell Res. Ther. 8, 14–28.10.1186/s13287-016-0465-2Search in Google Scholar PubMed PubMed Central

Amiri, F., Halabian, R., Harati, M.D., Bahadori, M., Mehdipour, A., Roushandeh, A.M., and Roudkenar, M.H. (2015). Positive selection of Wharton’s jelly-derived CD105⁺ cells by MACS technique and their subsequent cultivation under suspension culture condition: a simple, versatile culturing method to enhance the multipotentiality of mesenchymal stem cells. Hematology 20, 208–216.10.1179/1607845414Y.0000000185Search in Google Scholar PubMed

Atiyeh, B.S., El Khatib, A.M., and Dibo, S.A. (2013). Pressure garment therapy (PGT) of burn scars: evidence-based efficacy. Ann. Burns Fire Disasters 26, 205–212.Search in Google Scholar PubMed

Aung, L.L., Mouradian, M.M., Dhib-Jalbut, S., and Balashov, K.E. (2015). MMP-9 expression is increased in B lymphocytes during multiple sclerosis exacerbation and is regulated by microRNA-320a. J. Neuroimmunol. 278, 185–189.10.1016/j.jneuroim.2014.11.004Search in Google Scholar PubMed PubMed Central

Ayache, S.S. and Chalah, M.A. (2016). Stem cells therapy in multiple sclerosis – a new hope for progressive forms. J. Stem Cells Regen. Med. 12, 49–51.10.46582/jsrm.1201007Search in Google Scholar PubMed

Bai, L., Lennon, D.P., Eaton, V., Maier, K., Caplan, A.I., Miller, S.D., and Miller, R.H. (2009). Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 57, 1192–1203.10.1002/glia.20841Search in Google Scholar PubMed PubMed Central

Blakemore, W.F. (2008). Regeneration and repair in multiple sclerosis: the view of experimental pathology. J. Neurol. Sci. 265, 1–4.10.1016/j.jns.2007.03.006Search in Google Scholar PubMed

Bradl, M. and Lassmann, H. (2010). Oligodendrocytes: biology and pathology. Acta Neuropathol. 119, 37–53.10.1007/s00401-009-0601-5Search in Google Scholar PubMed PubMed Central

Buc, M. (2013). Role of regulatory T cells in pathogenesis and biological therapy of multiple sclerosis. Mediat. Inflamm. 2013, 963748.10.1155/2013/963748Search in Google Scholar PubMed PubMed Central

Buzanska, L., Machaj, E.K., Zablocka, B., Pojda, Z., and Domanska-Janik, K. (2002). Human cord blood-derived cells attain neuronal and glial features in vitro. J. Cell Sci. 115, 2131–2138.10.1242/jcs.115.10.2131Search in Google Scholar PubMed

Camps, A., Almolda, B., Gonzalez, B., and Castellano, B. (2016). Microimmunotherapeutic administration of cytokines improve the clinical symptoms in EAE an animal model of multiple sclerosis. Homeopathy 105, 10–10.10.1016/j.homp.2015.12.009Search in Google Scholar

Can, A. and Karahuseyinoglu, S. (2007). Concise review: human umbilical cord stroma with regard to the source of fetus-derived stem cells. Stem Cells 25, 2886–2895.10.1634/stemcells.2007-0417Search in Google Scholar PubMed

Carroll, P.D., Nankervis, C.A., Iams, J., and Kelleher, K. (2012). Umbilical cord blood as a replacement source for admission complete blood count in premature infants. J. Perinatol. 32, 97–102.10.1038/jp.2011.60Search in Google Scholar PubMed PubMed Central

Cheng, T., Yang, B., Li, D., Ma, S., Tian, Y., Qu, R., Zhang, W., Zhang, Y., Hu, K., Guan, F., et al. (2015). Wharton’s jelly transplantation improves neurologic function in a rat model of traumatic brain injury. Cell Mol. Neurobiol. 35, 641–649.10.1007/s10571-015-0159-9Search in Google Scholar PubMed PubMed Central

Costantino, C.M., Hutton, J., Baecher-Allan, C., and Hafler, D.A. (2008). Multiple sclerosis and regulatory T cells. J. Clin. Immunol. 28, 697–706.10.1007/s10875-008-9236-xSearch in Google Scholar PubMed PubMed Central

da Silva Meirelles, L., Chagastelles, P.C., and Nardi, N.B. (2006). Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 119, 2204–2213.10.1242/jcs.02932Search in Google Scholar PubMed

Dalla Libera, D., Di Mitri, D., Bergami, A., Centonze, D., Gasperini, C., Grasso, M.G., Galgani, S., Martinelli, V., Comi, G., Avolio, C., et al. (2011). T regulatory cells are markers of disease activity in multiple sclerosis patients. PLoS One 6, e21386.10.1371/journal.pone.0021386Search in Google Scholar PubMed PubMed Central

Davies, J.E., Walker, J.T., and Keating, A. (2017). Concise review: Wharton’s jelly: the rich, but enigmatic, source of mesenchymal stromal cells. Stem Cells Transl. Med. 6, 1620–1630.10.1002/sctm.16-0492Search in Google Scholar PubMed PubMed Central

Dhaeze, T., Peelen, E., Hombrouck, A., Peeters, L., Van Wijmeersch, B., Lemkens, N., Lemkens, P., Somers, V., Lucas, S., Broux, B., et al. (2015). Circulating follicular regulatory T cells are defective in multiple sclerosis. J. Immunol. 195, 832–840.10.4049/jimmunol.1500759Search in Google Scholar PubMed

Di Ianni, M., Del Papa, B., De Ioanni, M., Moretti, L., Bonifacio, E., Cecchini, D., Sportoletti, P., Falzetti, F., and Tabilio, A. (2008). Mesenchymal cells recruit and regulate T regulatory cells. Exp. Hematol. 36, 309–318.10.1016/j.exphem.2007.11.007Search in Google Scholar PubMed

Divya, M.S., Roshin, G.E., Divya, T.S., Rasheed, V.A., Santhoshkumar, T.R., Elizabeth, K.E., James, J., and Pillai, R.M. (2012). Umbilical cord blood-derived mesenchymal stem cells consist of a unique population of progenitors co-expressing mesenchymal stem cell and neuronal markers capable of instantaneous neuronal differentiation. Stem Cell Res. Ther. 3, 1–16.10.1186/scrt148Search in Google Scholar PubMed PubMed Central

Donders, R., Vanheusden, M., Bogie, J.F., Ravanidis, S., Thewissen, K., Stinissen, P., Gyselaers, W., Hendriks, J.J., and Hellings, N. (2015). Human Wharton’s jelly-derived stem cells display immunomodulatory properties and transiently improve rat experimental autoimmune encephalomyelitis. Cell Transplant. 24, 2077–2098.10.3727/096368914X685104Search in Google Scholar PubMed

Douvaras, P., Wang, J., Zimmer, M., Hanchuk, S., O’Bara, M.A., Sadiq, S., Sim, F.J., Goldman, J., and Fossati, V. (2014). Efficient generation of myelinating oligodendrocytes from primary progressive multiple sclerosis patients by induced pluripotent stem cells. Stem Cell Rep. 3, 250–259.10.1016/j.stemcr.2014.06.012Search in Google Scholar PubMed PubMed Central

Ebrahimi Kalan, A., Soleimani Rad, J., Kafami, L., Mohamadnezhad, D., Khaki, A.A., and Mohammadi Roushandeh, A. (2014). MS14, a marine herbal medicine, an immunosuppressive drug in experimental autoimmune encephalomyelitis. Iran. Red Crescent Med. J. 16, e16956.10.5812/ircmj.16956Search in Google Scholar PubMed PubMed Central

El Omar, R., Beroud, J., Stoltz, J.F., Menu, P., Velot, E., and Decot, V. (2014). Umbilical cord mesenchymal stem cells: the new gold standard for mesenchymal stem cell-based therapies? Tissue Eng. Part B Rev. 20, 523–544.10.1089/ten.teb.2013.0664Search in Google Scholar PubMed

English, K., Ryan, J., Tobin, L., Murphy, M., Barry, F., and Mahon, B.P. (2009). Cell contact, prostaglandin E2 and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4⁺ CD25 Highforkhead box P3⁺ regulatory T cells. Clin. Exp. Immunol. 156, 149–160.10.1111/j.1365-2249.2009.03874.xSearch in Google Scholar PubMed PubMed Central

Farzaneh Taban, Z., Khatibi, S., Halabian, R., and Mohammadi Roushandeh, A. (2016). The effects of preconditioning on survival of mesenchymal stem cells in vitro. Gene Cell Tissue 3, e40229.10.17795/gct-40229Search in Google Scholar

Fenollosa, R., Garcia-Rico, E., Alvarez, S., Alvarez, R., Yu, X., Rodriguez, I., Carregal-Romero, S., Villanueva, C., Garcia-Algar, M., Rivera-Gil, P., et al. (2014). Silicon particles as Trojan horses for potential cancer therapy. J. Nanobiotechnology. 12, 35–44.10.1186/s12951-014-0035-7Search in Google Scholar PubMed PubMed Central

Fonseka, M., Ramasamy, R., Tan, B.C., and Seow, H.F. (2012). Human umbilical cord blood-derived mesenchymal stem cells (hUCB-MSC) inhibit the proliferation of K562 (human erythromyeloblastoid leukaemic cell line). Cell Biol. Int. 36, 793–801.10.1042/CBI20110595Search in Google Scholar PubMed

Gajofatto, A. and Benedetti, M.D. (2015). Treatment strategies for multiple sclerosis: when to start, when to change, when to stop? World J. Clin. Cases 3, 545–555.10.12998/wjcc.v3.i7.545Search in Google Scholar PubMed PubMed Central

Grade, S., Bernardino, L., and Malva, J.O. (2013). Oligodendrogenesis from neural stem cells: perspectives for remyelinating strategies. Int. J. Dev. Neurosci. 31, 692–700.10.1016/j.ijdevneu.2013.01.004Search in Google Scholar PubMed

Guan, J.Z., Guan, W.P., and Maeda, T. (2018). Vitamin E administration erases an enhanced oxidation in multiple sclerosis. Can. J. Physiol. Pharmacol. 96, 1181–1183.10.1139/cjpp-2018-0246Search in Google Scholar PubMed

Harati, M.D., Amiri, F., Jaleh, F., Mehdipour, A., Harati, M.D., Molaee, S., Bahadori, M., Shokrgozar, M.A., Jalili, M.A., and Roudkenar, M.H. (2015). Targeting delivery of lipocalin 2-engineered mesenchymal stem cells to colon cancer in order to inhibit liver metastasis in nude mice. Tumour Biol. 36, 6011–6018.10.1007/s13277-015-3277-6Search in Google Scholar PubMed

Hedley, L. (2012). Multiple sclerosis treatment options. PJ. 288, 247–250.Search in Google Scholar

Hoang-Ngoc, M., Gebrane-Younes, J., Smadja, A., and Orcel, L. (1985). Structure and function of the fetal umbilical vessels. J. Gynecol. Obstet. Biol. Reprod. (Paris) 14, 973–979.Search in Google Scholar PubMed

Hou, Z.-L., Liu, Y., Mao, X.-H., Wei, C.-Y., Meng, M.-Y., Liu, Y.-H., Zhuyun Yang, Z., Zhu, H., Short, M., Bernard, C., et al. (2013). Transplantation of umbilical cord and bone marrow-derived mesenchymal stem cells in a patient with relapsing-remitting multiple sclerosis. Cell Adh. Migr. 7, 404–407.10.4161/cam.26941Search in Google Scholar PubMed PubMed Central

Ji, J., Ruan, J., and Cui, D. (2010). Advances of nanotechnology in the stem cells research and development. Nano. Biomed. Eng. 2, 67–90.10.5101/nbe.v2i1.p67-89Search in Google Scholar

Karahuseyinoglu, S., Cinar, O., Kilic, E., Kara, F., Akay, G.G., Demiralp, D.O., Tukun, A., Uckan, D., and Can, A. (2007). Biology of stem cells in human umbilical cord stroma: in situ and in vitro surveys. Stem Cells. 25, 319–331.10.1634/stemcells.2006-0286Search in Google Scholar PubMed

Kohm, A.P., Carpentier, P.A., Anger, H.A., and Miller, S.D. (2002). Cutting edge: CD4+ CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J. Immunol. 169, 4712–4716.10.4049/jimmunol.169.9.4712Search in Google Scholar PubMed

Kolf, C.M., Cho, E., and Tuan, R.S. (2007). Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res. Ther. 9, 204–204.10.1186/ar2116Search in Google Scholar PubMed PubMed Central

Korn, T. (2008). Pathophysiology of multiple sclerosis. J. Neurol. 255 (Suppl 6), 2–6.10.1007/s00415-008-6001-2Search in Google Scholar PubMed

Kuan, T.L.T., Amini, F., and Seghayat, M.S. (2017). Feasibility and toxicity of hematopoietic stem cell transplant in multiple sclerosis. Iran. J. Basic Med. Sci. 20, 729–738.Search in Google Scholar PubMed

Kubinova, S. and Sykova, E. (2010). Nanotechnologies in regenerative medicine. Minim Invasive Ther. Allied Technol. 19, 144–156.10.3109/13645706.2010.481398Search in Google Scholar PubMed

Kuchroo, P., Dave, V., Vijayan, A., Viswanathan, C., and Ghosh, D. (2015). Paracrine factors secreted by umbilical cord-derived mesenchymal stem cells induce angiogenesis in vitro by a VEGF-independent pathway. Stem Cells Dev. 24, 437–450.10.1089/scd.2014.0184Search in Google Scholar PubMed PubMed Central

Kyurkchiev, D., Bochev, I., Ivanova-Todorova, E., Mourdjeva, M., Oreshkova, T., Belemezova, K., and Kyurkchiev, S. (2014). Secretion of immunoregulatory cytokines by mesenchymal stem cells. World J. Stem Cells 6, 552–570.10.4252/wjsc.v6.i5.552Search in Google Scholar PubMed PubMed Central

Le Blanc, K. and Mougiakakos, D. (2012). Multipotent mesenchymal stromal cells and the innate immune system. Nat. Rev. Immunol. 12, 383–396.10.1038/nri3209Search in Google Scholar PubMed

Leite, C., Silva, N.T., Mendes, S., Ribeiro, A., de Faria, J.P., Lourenco, T., dos Santos, F., Andrade, P.Z., Cardoso, C.M., Vieira, M., et al. (2014). Differentiation of human umbilical cord matrix mesenchymal stem cells into neural-like progenitor cells and maturation into an oligodendroglial-like lineage. PLoS One 9, e111059.10.1371/journal.pone.0111059Search in Google Scholar PubMed PubMed Central

Li, J., Fan, C., Pei, H., Shi, J., and Huang, Q. (2013). Smart drug delivery nanocarriers with self-assembled DNA nanostructures. Adv. Mater. 25, 4386–4396.10.1002/adma.201300875Search in Google Scholar PubMed

Li, J.F., Zhang, D.J., Geng, T., Chen, L., Huang, H., Yin, H.L., Zhang, Y.Z., Lou, J.Y., Cao, B., and Wang, Y.L. (2014). The potential of human umbilical cord-derived mesenchymal stem cells as a novel cellular therapy for multiple sclerosis. Cell Transplant. 23, 113–122.10.3727/096368914X685005Search in Google Scholar PubMed

Li, T., Xia, M., Gao, Y., Chen, Y., and Xu, Y. (2015). Human umbilical cord mesenchymal stem cells: an overview of their potential in cell-based therapy. Expert Opin. Biol. Ther. 15, 1293–1306.10.1517/14712598.2015.1051528Search in Google Scholar PubMed

Liang, J., Zhang, H., Hua, B., Wang, H., Wang, J., Han, Z., and Sun, L. (2009). Allogeneic mesenchymal stem cells transplantation in treatment of multiple sclerosis. Mult. Scler. 15, 644–646.10.1177/1352458509104590Search in Google Scholar PubMed

Liu, R., Zhang, Z., Lu, Z., Borlongan, C., Pan, J., Chen, J., Qian, L., Liu, Z., Zhu, L., Zhang, J., et al. (2013). Human umbilical cord stem cells ameliorate experimental autoimmune encephalomyelitis by regulating immunoinflammation and remyelination. Stem Cells Dev. 22, 1053–1062.10.1089/scd.2012.0463Search in Google Scholar PubMed

Liu, Q., Zheng, H., Chen, X., Peng, Y., Huang, W., Li, X., Li, G., Xia, W., Sun, Q., and Xiang, A.P. (2015). Human mesenchymal stromal cells enhance the immunomodulatory function of CD8(+)CD28(-) regulatory T cells. Cell Mol. Immunol. 12, 708–718.10.1038/cmi.2014.118Search in Google Scholar PubMed PubMed Central

Luz-Crawford, P., Kurte, M., Bravo-Alegría, J., Contreras, R., Nova-Lamperti, E., Tejedor, G., Noël, D., Jorgensen, C., Figueroa, F., Djouad, F., et al. (2013). Mesenchymal stem cells generate a CD4⁺CD25⁺Foxp3⁺ regulatory T cell population during the differentiation process of Th1 and Th17 cells. Stem Cell Res. Ther. 4, 65–76.10.1186/scrt216Search in Google Scholar PubMed PubMed Central

Lv, M., Zhang, Y., Liang, L., Wei, M., Hu, W., Li, X., and Huang, Q. (2012). Effect of graphene oxide on undifferentiated and retinoic acid-differentiated SH-SY5Y cells line. Nanoscale 4, 3861–3866.10.1039/c2nr30407dSearch in Google Scholar PubMed

Ma, S., Liang, S., Jiao, H., Chi, L., Shi, X., Tian, Y., Yang, B., and Guan, F. (2014). Human umbilical cord mesenchymal stem cells inhibit C6 glioma growth via secretion of dickkopf-1 (DKK1). Mol. Cell Biochem. 385, 277–286.10.1007/s11010-013-1836-ySearch in Google Scholar PubMed

Martino, G., Franklin, R.J., Baron Van Evercooren, A., and Kerr, D.A. (2010). Stem cell transplantation in multiple sclerosis: current status and future prospects. Nat. Rev. Neurol. 6, 247–255.10.1038/nrneurol.2010.35Search in Google Scholar PubMed

Mayer, F.A. (1996). Wharton’s jelly of the umbilical cord. In: Extracellular matrix: tissue function. (Netherlands: Comper, W.D. CRC Press), pp. 443–448.Search in Google Scholar

Meng, M., Liu, Y., Wang, W., Wei, C., Liu, F., Du, Z., Xie, Y., Tang, W., Hou, Z., and Li, Q. (2018). Umbilical cord mesenchymal stem cell transplantation in the treatment of multiple sclerosis. Am. J. Transl. Res. 10, 212–223.Search in Google Scholar PubMed

Nakamura, Y., Tanaka, Y., Ando, T., Sato, Y., Yujiri, T., and Tanizawa, Y. (2007). Successful engraftment of the second reduced-intensity conditioning cord blood transplantation (CBT) for a patient who developed graft rejection and infectious complications after the first CBT for AML. Bone Marrow Transplant. 40, 395–396.10.1038/sj.bmt.1705732Search in Google Scholar PubMed

Nanaev, A.K., Kohnen, G., Milovanov, A.P., Domogatsky, S.P., and Kaufmann, P. (1997). Stromal differentiation and architecture of the human umbilical cord. Placenta 18, 53–64.10.1016/S0143-4004(97)90071-0Search in Google Scholar PubMed

National Multiple Sclerosis Society. (2018). Umbilical cord blood donation. Available at: https://www.nationalmssociety.org/Research/Participate-in-Research-Studies/Donate-to-Tissue-Banks/Umbilical-Cord-Blood-Donation. Accessed: 8 Jul 2018.Search in Google Scholar

Nejati-Koshki, K., Pilehvar-Soltanahmadi, Y., Alizadeh, E., Ebrahimi-Kalan, A., Mortazavi, Y., and Zarghami, N. (2017). Development of emu oil-loaded PCL/collagen bioactive nanofibers for proliferation and stemness preservation of human adipose-derived stem cells: possible application in regenerative medicine. Drug. Dev. Ind. Pharm. 43, 1978–1988.10.1080/03639045.2017.1357731Search in Google Scholar PubMed

Nicaise, A.M., Johnson, K.M., Willis, C.M., Guzzo, R.M., and Crocker, S.J. (2018). TIMP-1 promotes oligodendrocyte differentiation through receptor-mediated signaling. Mol. Neurobiol., DOI: 10.1007/s12035-018-1310-7. [Epub ahead of print]10.1007/s12035-018-1310-7Search in Google Scholar PubMed

Nikbin, B., Bonab, M.M., and Talebian, F. (2007). Microchimerism and stem cell transplantation in multiple sclerosis. Int. Rev. Neurobiol. 79, 173–202.10.1016/S0074-7742(07)79008-6Search in Google Scholar PubMed

Noori-Zadeh, A., Mesbah-Namin, S.A., Bistoon-beigloo, S., Bakhtiyari, S., Abbaszadeh, H.-A., Darabi, S., Rajabibazl, M., and Abdanipour, A. (2016). Regulatory T cell number in multiple sclerosis patients: a meta-analysis. Mult. Scler. Relat. Disord. 5, 73–76.10.1016/j.msard.2015.11.004Search in Google Scholar PubMed

Oh, D.Y., Cui, P., Hosseini, H., Mosse, J., Toh, B.H., and Chan, J. (2012). Potently immunosuppressive 5-fluorouracil-resistant mesenchymal stromal cells completely remit an experimental autoimmune disease. J. Immunol. 188, 2207–2217.10.4049/jimmunol.1101040Search in Google Scholar PubMed

Okada, H. and Khoury, S.J. (2012). Type17 T-cells in central nervous system autoimmunity and tumors. J. Clin. Immunol. 32, 802–808.10.1007/s10875-012-9686-zSearch in Google Scholar PubMed PubMed Central

Onwuha-Ekpete, L.C., Tokmina-Roszyk, D., and Fields, G.B. (2016). Selective inhibition of matrix metalloproteinase-9 reduces clinical severity in a murine model of multiple sclerosis via a reduced immune response. J. Immunol. 196, 139.112-139.112.10.4049/jimmunol.196.Supp.139.12Search in Google Scholar

Plantone, D., Renna, R., Sbardella, E., and Koudriavtseva, T. (2015). Concurrence of multiple sclerosis and brain tumors. Front. Neurol. 6, 40–43.10.3389/fneur.2015.00040Search in Google Scholar PubMed PubMed Central

Qiu, J., Zhang, R., Li, J., Sang, Y., Tang, W., Rivera Gil, P., and Liu, H. (2015). Fluorescent graphene quantum dots as traceable, pH-sensitive drug delivery systems. Int. J. Nanomed. 10, 6709–6724.10.2147/IJN.S91864Search in Google Scholar PubMed PubMed Central

Rafieemehr, H., Kheirandish, M., and Soleimani, M. (2015). Improving the neuronal differentiation efficiency of umbilical cord blood-derived mesenchymal stem cells cultivated under appropriate conditions. Iran. J. Basic Med. Sci. 18, 1100–1106.10.17795/ajmb-29066Search in Google Scholar PubMed

Revilla, A., Gonzalez, C., Iriondo, A., Fernandez, B., Prieto, C., Marin, C., and Liste, I. (2016). Current advances in the generation of human iPS cells: implications in cell-based regenerative medicine. J. Tissue Eng. Regen. Med. 10, 893–907.10.1002/term.2021Search in Google Scholar PubMed

Riordan, N.H., Morales, I., Fernandez, G., Allen, N., Fearnot, N.E., Leckrone, M.E., Markovich, D.J., Mansfield, D., Avila, D., Patel, A.N., et al. (2018). Clinical feasibility of umbilical cord tissue-derived mesenchymal stem cells in the treatment of multiple sclerosis. J. Transl. Med. 16, 57–68.10.1186/s12967-018-1433-7Search in Google Scholar PubMed PubMed Central

Ruenraroengsak, P., Chen, S., Hu, S., Melbourne, J., Sweeney, S., Thorley, A.J., Skepper, J.N., Shaffer, M.S., Tetley, T.D., and Porter, A.E. (2016). Translocation of functionalized multi-walled carbon nanotubes across human pulmonary alveolar epithelium: dominant role of epithelial type 1 cells. ACS Nano 10, 5070–5085.10.1021/acsnano.5b08218Search in Google Scholar PubMed PubMed Central

Sakaguchi, S. (2004). Naturally arising CD4⁺ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22, 531–562.10.1146/annurev.immunol.21.120601.141122Search in Google Scholar PubMed

Samadikuchaksaraei, A., Mehdipour, A., Habibi Roudkenar, M., Verdi, J., Joghataei, M.T., As’adi, K., Amiri, F., Dehghan Harati, M., Gholipourmalekabadi, M., and Karkuki Osguei, N. (2016). A dermal equivalent engineered with TGF-beta3 expressing bone marrow stromal cells and amniotic membrane: cosmetic healing of full-thickness skin wounds in rats. Artif Organs 40, E266–E279.10.1111/aor.12807Search in Google Scholar PubMed

Sanmano, B., Mizoguchi, M., Suga, Y., Ikeda, S., and Ogawa, H. (2005). Engraftment of umbilical cord epithelial cells in athymic mice: in an attempt to improve reconstructed skin equivalents used as epithelial composite. J. Dermatol. Sci. 37, 29–39.10.1016/j.jdermsci.2004.10.008Search in Google Scholar PubMed

Sarugaser, R., Hanoun, L., Keating, A., Stanford, W.L., and Davies, J.E. (2009). Human mesenchymal stem cells self-renew and differentiate according to a deterministic hierarchy. PLoS One 4, e6498.10.1371/journal.pone.0006498Search in Google Scholar PubMed PubMed Central

Satoh, N., Takenouchi, S., Hashimoto, S., Fujiwara, M., and Koike, T. (2007). Switching of donor cells after urgent second cord blood transplantation for suspected graft failure. Int. J. Hematol. 86, 451–454.10.1007/BF02984004Search in Google Scholar PubMed

Schmidt, N.O., Przylecki, W., Yang, W., Ziu, M., Teng, Y., Kim, S.U., Black, P.M., Aboody, K.S., and Carroll, R.S. (2005). Brain tumor tropism of transplanted human neural stem cells is induced by vascular endothelial growth factor. Neoplasia 7, 623–630.10.1593/neo.04781Search in Google Scholar PubMed PubMed Central

Sher, F., Balasubramaniyan, V., Boddeke, E., and Copray, S. (2008a). Oligodendrocyte differentiation and implantation: new insights for remyelinating cell therapy. Curr. Opin. Neurol. 21, 607–614.10.1097/WCO.0b013e32830f1e50Search in Google Scholar PubMed

Sher, F., Rossler, R., Brouwer, N., Balasubramaniyan, V., Boddeke, E., and Copray, S. (2008b). Differentiation of neural stem cells into oligodendrocytes: involvement of the polycomb group protein Ezh2. Stem Cells 26, 2875–2883.10.1634/stemcells.2008-0121Search in Google Scholar PubMed

Shirazi, H.A., Rasouli, J., Ciric, B., Rostami, A., and Zhang, G.-X. (2015). 1,25-Dihydroxyvitamin D3 enhances neural stem cell proliferation and oligodendrocyte differentiation. Exp. Mol. Pathol. 98, 240–245.10.1016/j.yexmp.2015.02.004Search in Google Scholar PubMed PubMed Central

Shiri-Shahsavar, M.R., Mirshafiee, A., Parastouei, K., Ebrahimi-Kalan, A., Yekaninejad, S., Soleymani, F., Chahardoli, R., Mazaheri Nezhad Fard, R., and Saboor-Yaraghi, A.A. (2016). A novel combination of docosahexaenoic acid, all-trans retinoic acid, and 1, 25-dihydroxyvitamin d3 reduces T-Bet gene expression, serum interferon gamma, and clinical scores but promotes ppargamma gene expression in experimental autoimmune encephalomyelitis. J. Mol. Neurosci. 60, 498–508.10.1007/s12031-016-0834-4Search in Google Scholar PubMed

Shroff, G. (2018). A review on stem cell therapy for multiple sclerosis: special focus on human embryonic stem cells. Stem Cells Cloning 11, 1–11.10.2147/SCCAA.S135415Search in Google Scholar PubMed PubMed Central

Song, B., Sun, G., Herszfeld, D., Sylvain, A., Campanale, N.V., Hirst, C.E., Caine, S., Parkington, H.C., Tonta, M.A., Coleman, H.A., et al. (2012). Neural differentiation of patient specific iPS cells as a novel approach to study the pathophysiology of multiple sclerosis. Stem Cell Res. 8, 259–273.10.1016/j.scr.2011.12.001Search in Google Scholar PubMed

Sorensen, P.S. (2014). New management algorithms in multiple sclerosis. Curr. Opin. Neurol. 27, 246–259.10.1097/WCO.0000000000000096Search in Google Scholar PubMed

Speiran, K., Bailey, D.P., Fernando, J., Macey, M., Barnstein, B., Kolawole, M., Curley, D., Watowich, S.S., Murray, P.J., Oskeritzian, C., et al. (2009). Endogenous suppression of mast cell development and survival by IL-4 and IL-10. J. Leukoc. Biol. 85, 826–836.10.1189/jlb.0708448Search in Google Scholar PubMed PubMed Central

Sturm, D., Gurevitz, S.L., and Turner, A. (2014). Multiple sclerosis: a review of the disease and treatment options. Consult. Pharm. 29, 469–479.10.4140/TCP.n.2014.469Search in Google Scholar PubMed

Sullivan, M.J. (2008). Banking on cord blood stem cells. Nat. Rev. Cancer. 8, 555–563.10.1038/nrc2418Search in Google Scholar PubMed

Sun, L., Wang, D., Liang, J., Zhang, H., Feng, X., Wang, H., Hua, B., Liu, B., Ye, S., Hu, X., et al. (2010). Umbilical cord mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus. Arthritis Rheum. 62, 2467–2475.10.1002/art.27548Search in Google Scholar PubMed

Sun, T. and Ma, Q.-H. (2013). Repairing neural injuries using human umbilical cord blood. Mol. Neurobiol. 47, 938–945.10.1007/s12035-012-8388-0Search in Google Scholar PubMed PubMed Central

Svobodova, E., Krulova, M., Zajicova, A., Pokorna, K., Prochazkova, J., Trosan, P., and Holan, V. (2012). The role of mouse mesenchymal stem cells in differentiation of naive T-cells into anti-inflammatory regulatory T-cell or proinflammatory helper T-cell 17 population. Stem Cells Dev. 21, 901–910.10.1089/scd.2011.0157Search in Google Scholar PubMed PubMed Central

Swamynathan, P., Venugopal, P., Kannan, S., Thej, C., Kolkundar, U., Bhagwat, S., Ta, M., Majumdar, A.S., and Balasubramanian, S. (2014). Are serum-free and xeno-free culture conditions ideal for large scale clinical grade expansion of Wharton’s jelly derived mesenchymal stem cells? A comparative study. Stem Cell Res. Ther. 5, 88–104.10.1186/scrt477Search in Google Scholar PubMed PubMed Central

Tipnis, S., Viswanathan, C., and Majumdar, A.S. (2010). Immunosuppressive properties of human umbilical cord-derived mesenchymal stem cells: role of B7-H1 and IDO. Immunol. Cell Biol. 88, 795–806.10.1038/icb.2010.47Search in Google Scholar PubMed

Todeschi, M.R., El Backly, R., Capelli, C., Daga, A., Patrone, E., Introna, M., Cancedda, R., and Mastrogiacomo, M. (2015). Transplanted umbilical cord mesenchymal stem cells modify the in vivo microenvironment enhancing angiogenesis and leading to bone regeneration. Stem Cells Dev. 24, 1570–1581.10.1089/scd.2014.0490Search in Google Scholar PubMed PubMed Central

Tondreau, T., Meuleman, N., Delforge, A., Dejeneffe, M., Leroy, R., Massy, M., Mortier, C., Bron, D., and Lagneaux, L. (2005). Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells 23, 1105–1112.10.1634/stemcells.2004-0330Search in Google Scholar PubMed

Tong, C.K., Vellasamy, S., Tan, B.C., Abdullah, M., Vidyadaran, S., Seow, H.F., and Ramasamy, R. (2011). Generation of mesenchymal stem cell from human umbilical cord tissue using a combination enzymatic and mechanical disassociation method. Cell Biol. Int. 35, 221–226.10.1042/CBI20100326Search in Google Scholar PubMed

Vizza, E., Correr, S., Goranova, V., Heyn, R., Angelucci, P.A., Forleo, R., and Motta, P.M. (1996). The collagen skeleton of the human umbilical cord at term. A scanning electron microscopy study after 2N-NaOH maceration. Reprod. Fertil. Dev. 8, 885–894.10.1071/RD9960885Search in Google Scholar PubMed

von Kaisenberg, C.S., Krenn, V., Ludwig, M., Nicolaides, K.H., and Brand-Saberi, B. (1998). Morphological classification of nuchal skin in human fetuses with trisomy 21, 18, and 13 at 12–18 weeks and in a trisomy 16 mouse. Anat. Embryol. (Berl.) 197, 105–124.10.1007/s004290050123Search in Google Scholar PubMed

Wang, Z., Ruan, J., and Cui, D. (2009a). Advances and prospect of nanotechnology in stem cells. Nanoscale Res. Lett. 4, 593–605.10.1007/s11671-009-9292-zSearch in Google Scholar PubMed PubMed Central

Wang, M., Yang, Y., Yang, D., Luo, F., Liang, W., Guo, S., and Xu, J. (2009b). The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro. Immunology 126, 220–232.10.1111/j.1365-2567.2008.02891.xSearch in Google Scholar PubMed PubMed Central

Wang, S., Bates, J., Li, X., Schanz, S., Chandler-Militello, D., Levine, C., Maherali, N., Studer, L., Hochedlinger, K., Windrem, M., et al. (2013). Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 12, 252–264.10.1016/j.stem.2012.12.002Search in Google Scholar PubMed PubMed Central

Wang, Y., Chen, X., Cao, W., and Shi, Y. (2014). Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat. Immunol. 15, 1009–1016.10.1038/ni.3002Search in Google Scholar PubMed

Wang, W., Deng, Z., Xu, X., Li, Z., Jung, F., Ma, N., and Lendlein, A. (2017a). Functional nanoparticles and their interactions with mesenchymal stem cells. Curr. Pharm. Des. 23, 3814–3832.10.2174/1381612823666170622110654Search in Google Scholar PubMed

Wang, D., Huang, S., Yuan, X., Liang, J., Xu, R., Yao, G., Feng, X., and Sun, L. (2017b). The regulation of the Treg/Th17 balance by mesenchymal stem cells in human systemic lupus erythematosus. Cell Mol. Immunol. 14, 423–431.10.1038/cmi.2015.89Search in Google Scholar PubMed PubMed Central

Watson, N., Divers, R., Kedar, R., Mehindru, A., Mehindru, A., Borlongan, M.C., and Borlongan, C.V. (2015). Discarded Wharton jelly of the human umbilical cord: a viable source for mesenchymal stromal cells. Cytotherapy 17, 18–24.10.1016/j.jcyt.2014.08.009Search in Google Scholar PubMed PubMed Central

Wei, M., Chen, N., Li, J., Yin, M., Liang, L., He, Y., Song, H., Fan, C., and Huang, Q. (2012). Polyvalent immunostimulatory nanoagents with self-assembled CpG oligonucleotide-conjugated gold nanoparticles. Angew. Chem. Int. Ed. 51, 1202–1206.10.1002/anie.201105187Search in Google Scholar PubMed

Weiss, M.L., Anderson, C., Medicetty, S., Seshareddy, K.B., Weiss, R.J., VanderWerff, I., Troyer, D., and McIntosh, K.R. (2008). Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells 26, 2865–2874.10.1634/stemcells.2007-1028Search in Google Scholar PubMed

Xu, C., Yu, P., Han, X., Du, L., Gan, J., Wang, Y., and Shi, Y. (2014). TGF-β promotes immune responses in the presence of mesenchymal stem cells. J. Immunol. 192, 103–109.10.4049/jimmunol.1302164Search in Google Scholar PubMed

Yang, D., Li, T., Xu, M., Gao, F., Yang, J., Yang, Z., and Le, W. (2014). Graphene oxide promotes the differentiation of mouse embryonic stem cells to dopamine neurons. Nanomedicine (Lond.) 9, 2445–2455.10.2217/nnm.13.197Search in Google Scholar PubMed

Yang, H., Sun, J., Wang, F., Li, Y., Bi, J., and Qu, T. (2016). Umbilical cord-derived mesenchymal stem cells reversed the suppressive deficiency of T regulatory cells from peripheral blood of patients with multiple sclerosis in a co-culture – a preliminary study. Oncotarget 7, 72537–72545.10.18632/oncotarget.12345Search in Google Scholar PubMed PubMed Central

Ye, Z., Wang, Y., Xie, H.Y., and Zheng, S.S. (2008). Immunosuppressive effects of rat mesenchymal stem cells: involvement of CD4⁺CD25⁺ regulatory T cells. Hepatobiliary Pancreat Dis. Int. 7, 608–614.Search in Google Scholar PubMed

You, D.G., Deepagan, V.G., Um, W., Jeon, S., Son, S., Chang, H., Yoon, H.I., Cho, Y.W., Swierczewska, M., Lee, S., et al. (2016). ROS-generating TiO2 nanoparticles for non-invasive sonodynamic therapy of cancer. Sci. Rep. 6, 23200.10.1038/srep23200Search in Google Scholar PubMed PubMed Central

Zhang, R., Lee, P., Lui, V.C., Chen, Y., Liu, X., Lok, C.N., To, M., Yeung, K.W., and Wong, K.K. (2015). Silver nanoparticles promote osteogenesis of mesenchymal stem cells and improve bone fracture healing in osteogenesis mechanism mouse model. Nanomedicine 11, 1949–1959.10.1016/j.nano.2015.07.016Search in Google Scholar PubMed

Zhang, Z., Sun, Q., Zhong, J., Yang, Q., Li, H., Du, C., Liang, B., and Shuai, X. (2014). Magnetic resonance imaging-visible and pH-sensitive polymeric micelles for tumor targeted drug delivery. J. Biomed. Nanotechnol. 10, 216–226.10.1166/jbn.2014.1729Search in Google Scholar PubMed

Zozulya, A.L. and Wiendl, H. (2008). The role of regulatory T cells in multiple sclerosis. Nat. Clin. Pract. Neurol. 4, 384–398.10.1038/ncpneuro0832Search in Google Scholar PubMed