Stem cell transplantation therapy in Parkinson’s disease
Identifieur interne : 000522 ( Ncbi/Merge ); précédent : 000521; suivant : 000523Stem cell transplantation therapy in Parkinson’s disease
Auteurs : Mu Fu [Taïwan] ; Chia Li [Taïwan] ; Hsiu Lin [Taïwan] ; Pei Chen [Taïwan] ; Marcus Calkins [Taïwan] ; Yu Chang [Taïwan] ; Pei Cheng [Taïwan] ; Shang Yang [Taïwan]Source :
- SpringerPlus ; 2015.
Abstract
Ineffective therapeutic treatments and inadequate repair ability in the central nervous system are disturbing problems for several neurological diseases. Fortunately, the development of clinically applicable populations of stem cells has provided an avenue to overcome the failure of endogenous repair systems and substitute new cells into the damaged brain. However, there are still several existing obstacles to translating into clinical application. Here we review the stem-cell based therapies for Parkinson’s disease and discuss the potential advantages and drawbacks. We hope this review may provide suggestions for viable strategies to overcome the current technical and biological issues associated with the application of stem cells in Parkinson’s disease.
Url:
DOI: 10.1186/s40064-015-1400-1
PubMed: 26543732
PubMed Central: 4628010
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Tainan</wicri:regionArea><wicri:noRegion>Tainan</wicri:noRegion></affiliation></author><author><name sortKey="Calkins, Marcus J" sort="Calkins, Marcus J" uniqKey="Calkins M" first="Marcus" last="Calkins">Marcus Calkins</name><affiliation wicri:level="1"><nlm:aff id="Aff3">Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan, 70101 Taiwan</nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea>Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan</wicri:regionArea><wicri:noRegion>Tainan</wicri:noRegion></affiliation></author><author><name sortKey="Chang, Yu Fan" sort="Chang, Yu Fan" uniqKey="Chang Y" first="Yu" last="Chang">Yu Chang</name><affiliation wicri:level="1"><nlm:aff id="Aff2">Department of Physiology, College of Medicine, National Cheng Kung University, Tainan, 70101 Taiwan</nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea>Department of Physiology, College of Medicine, 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Sciences, College of Medicine, National Cheng Kung University, Tainan</wicri:regionArea><wicri:noRegion>Tainan</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff2">Department of Physiology, College of Medicine, National Cheng Kung University, Tainan, 70101 Taiwan</nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea>Department of Physiology, College of Medicine, National Cheng Kung University, Tainan</wicri:regionArea><wicri:noRegion>Tainan</wicri:noRegion></affiliation></author></analytic><series><title level="j">SpringerPlus</title><idno type="e-ISSN">2193-1801</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Ineffective therapeutic treatments and inadequate repair ability in the central nervous system are disturbing problems for several neurological diseases. Fortunately, the development of clinically applicable populations of stem cells has provided an avenue to overcome the failure of endogenous repair systems and substitute new cells into the damaged brain. However, there are still several existing obstacles to translating into clinical application. Here we review the stem-cell based therapies for Parkinson’s disease and discuss the potential advantages and drawbacks. We hope this review may provide suggestions for viable strategies to overcome the current technical and biological issues associated with the application of stem cells in Parkinson’s disease.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Aleynik, A" uniqKey="Aleynik A">A Aleynik</name></author><author><name sortKey="Gernavage, Km" uniqKey="Gernavage K">KM Gernavage</name></author><author><name sortKey="Mourad, Y" uniqKey="Mourad Y">Y Mourad</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Anderson, L" uniqKey="Anderson L">L Anderson</name></author><author><name sortKey="Burnstein, Rm" uniqKey="Burnstein R">RM Burnstein</name></author><author><name sortKey="He, X" uniqKey="He X">X He</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Badger, Jl" uniqKey="Badger J">JL Badger</name></author><author><name sortKey="Cordero Llana, O" uniqKey="Cordero Llana O">O 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Springerplus</journal-id><journal-id journal-id-type="iso-abbrev">Springerplus</journal-id><journal-title-group><journal-title>SpringerPlus</journal-title></journal-title-group><issn pub-type="epub">2193-1801</issn><publisher><publisher-name>Springer International Publishing</publisher-name><publisher-loc>Cham</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26543732</article-id><article-id pub-id-type="pmc">4628010</article-id><article-id pub-id-type="publisher-id">1400</article-id><article-id pub-id-type="doi">10.1186/s40064-015-1400-1</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Stem cell transplantation therapy in Parkinson’s disease</article-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Fu</surname><given-names>Mu-Hui</given-names></name><address><email>kf4089@gmail.com</email></address><xref ref-type="aff" rid="Aff1"></xref><xref ref-type="aff" rid="Aff4"></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Li</surname><given-names>Chia-Ling</given-names></name><address><email>lingboxer@gmail.com</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Lin</surname><given-names>Hsiu-Lien</given-names></name><address><email>hllin@mail.tlri.gov.tw</email></address><xref ref-type="aff" rid="Aff1"></xref><xref ref-type="aff" rid="Aff5"></xref></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Pei-Chun</given-names></name><address><email>pcchen@mail.ncku.edu.tw</email></address><xref ref-type="aff" rid="Aff1"></xref><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Calkins</surname><given-names>Marcus J.</given-names></name><address><email>mjcalkins@mail.ncku.edu.tw</email></address><xref ref-type="aff" rid="Aff3"></xref></contrib><contrib contrib-type="author"><name><surname>Chang</surname><given-names>Yu-Fan</given-names></name><address><email>yfchang421@gmail.com</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Cheng</surname><given-names>Pei-Hsun</given-names></name><address><email>peihsunmail@yahoo.com.tw</email></address><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Yang</surname><given-names>Shang-Hsun</given-names></name><address><phone>+886-6-2353535</phone><email>syang@mail.ncku.edu.tw</email></address><xref ref-type="aff" rid="Aff1"></xref><xref ref-type="aff" rid="Aff2"></xref></contrib><aff id="Aff1"><label></label>Institute of Basic Medical Sciences, College of Medicine, National Cheng Kung University, Tainan, 70101 Taiwan</aff><aff id="Aff2"><label></label>Department of Physiology, College of Medicine, National Cheng Kung University, Tainan, 70101 Taiwan</aff><aff id="Aff3"><label></label>Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan, 70101 Taiwan</aff><aff id="Aff4"><label></label>Department of Neurology, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung, 83301 Taiwan</aff><aff id="Aff5"><label></label>Division of Breeding and Genetics, Livestock Research Institute, Council of Agriculture, Tainan, 71246 Taiwan</aff></contrib-group><pub-date pub-type="epub"><day>13</day><month>10</month><year>2015</year></pub-date><pub-date pub-type="pmc-release"><day>13</day><month>10</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>4</volume><elocation-id>597</elocation-id><history><date date-type="received"><day>9</day><month>8</month><year>2015</year></date><date date-type="accepted"><day>6</day><month>10</month><year>2015</year></date></history><permissions><copyright-statement>© Fu et al. 2015</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold>This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.</license-p></license></permissions><abstract id="Abs1"><p>Ineffective therapeutic treatments and inadequate repair ability in the central nervous system are disturbing problems for several neurological diseases. Fortunately, the development of clinically applicable populations of stem cells has provided an avenue to overcome the failure of endogenous repair systems and substitute new cells into the damaged brain. However, there are still several existing obstacles to translating into clinical application. Here we review the stem-cell based therapies for Parkinson’s disease and discuss the potential advantages and drawbacks. We hope this review may provide suggestions for viable strategies to overcome the current technical and biological issues associated with the application of stem cells in Parkinson’s disease.</p></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Stem cells</kwd><kwd>Cell replacement therapy</kwd><kwd>Neurodegenerative disease</kwd><kwd>Parkinson’s disease</kwd></kwd-group><funding-group><award-group><funding-source><institution>Ministry of Education, Taiwan</institution></funding-source><award-id>The Aim for the Top University Project</award-id><principal-award-recipient><name><surname>Yang</surname><given-names>Shang-Hsun</given-names></name></principal-award-recipient></award-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100004663</institution-id><institution>Ministry of Science and Technology, Taiwan (TW)</institution></institution-wrap></funding-source><award-id>MOST 102-2628-B-006-010-MY3</award-id><award-id>MOST 103-2320-B-006 -010</award-id><principal-award-recipient><name><surname>Yang</surname><given-names>Shang-Hsun</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2015</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1" sec-type="introduction"><title>Background</title><p>Stem cells are undifferentiated cells that are able to differentiate into multiple specialized cell types. Since stem cells have the potential to replace or restore lost cells, they have been evaluated and considered as potential therapeutic agents in neuronal diseases. Numerous studies have focused on stem cell therapy in spinal cord injury, spinal muscular atrophy, brain ischemia, amyotrophic lateral sclerosis and other neurodegenerative diseases (Nicaise et al. <xref ref-type="bibr" rid="CR67">2015</xref>; Mendonca et al. <xref ref-type="bibr" rid="CR61">2015</xref>; Lukovic et al. <xref ref-type="bibr" rid="CR55">2015</xref>; Frattini et al. <xref ref-type="bibr" rid="CR21">2015</xref>; Ju et al. <xref ref-type="bibr" rid="CR36">2014</xref>). Because neurodegenerative diseases are often associated with regional cell loss, cell transplantation therapies may effectively restore and replace cells in the damaged tissues. Therefore, we will highlight several milestones in the development of stem cell therapy for Parkinson’s disease (PD), which is the second most common neurodegenerative diseases.</p></sec><sec id="Sec2"><title>Characteristics of various stem cells for therapy</title><p>There are several types of stem cells under consideration for therapeutic purposes. Below we will introduce four kinds of stem cells, including embryonic stem cells (ES cells), induced pluripotent stem cells (iPSCs), neural stem cells (NSCs) and mesenchymal stem cells (MSCs).</p><sec id="Sec3"><title>Embryonic stem cells (ES cells)</title><p>ES cells are pluripotent cells derived from the inner cell mass (ICM) of blastocysts. These cells are able to differentiate into three germ layers, and subsequently may be driven to develop into many different types of cells (Thomson et al. <xref ref-type="bibr" rid="CR91">1998</xref>). In neuronal systems, prior studies have showed that functional neurons, astrocytes, and oligodendrocytes could be derived from ES cells in vitro (Wichterle et al. <xref ref-type="bibr" rid="CR98">2002</xref>; Zhang et al. <xref ref-type="bibr" rid="CR104">2001</xref>). As a result, ES cells transplant has been widely suggested in several neurodegenerative diseases or brain injuries (Aleynik et al. <xref ref-type="bibr" rid="CR1">2014</xref>). However, their high capacity of self-renewing and pluripotency lead to high risk of tumor formation, especially teratoma (Gordeeva <xref ref-type="bibr" rid="CR27">2011</xref>). Another major limitation is the ethical issue regarding their origin. Isolating ICM from blastocysts destroys early embryos and raises the moral concern (Daar and Sheremeta <xref ref-type="bibr" rid="CR15">2003</xref>). Due to the high tumorigenicity and ethical considerations, non-ES cells have become a major focus of cell-based therapies, such as adult stem cells.</p></sec><sec id="Sec4"><title>Induced pluripotent stem cells (iPSCs)</title><p>In 2006, Kazutoshi Takahashi and Shinya Yamanaka established the induced pluripotent stem cells, which are ES-like cells transformed from fibroblasts (Takahashi and Yamanaka <xref ref-type="bibr" rid="CR86">2006</xref>). This method is accomplished by introducing four transcription factor genes encoding Oct4, Sox2, Klf4, and c-Myc into skin fibroblasts. Since iPSCs may be derived directly from adult tissues, the risk of immune rejection and complicated ethical issues are avoided when used as a substrate for transplantation. Therefore, iPSCs were recently used as a potential cell source to repair neuronal networks in various CNS diseases, such as ischemic stroke and PD (Wernig et al. <xref ref-type="bibr" rid="CR97">2008</xref>; Yuan et al. <xref ref-type="bibr" rid="CR103">2013</xref>).</p><p>However, one major drawback of the iPSC technology is that c-Myc is well-defined as an oncogene, and reactivation of c-Myc increases the risk of tumor formation (Kawai et al. <xref ref-type="bibr" rid="CR37">2010</xref>). Yamanaka et al. modified the reprogramming protocol by using only Oct4, Sox2 and Klf4 without c-Myc, and it significantly decreased the tumorigenicity; however, this modified method significantly reduced the efficiency of iPSC formation (Nakagawa et al. <xref ref-type="bibr" rid="CR66">2008</xref>). Furthermore, Oct4, Sox2 and Klf4 are overexpressed or activated in various types of cancer as well (Peng et al. <xref ref-type="bibr" rid="CR73">2010</xref>; Raguel et al. <xref ref-type="bibr" rid="CR78">2009</xref>; Sholl et al. <xref ref-type="bibr" rid="CR83">2010</xref>), suggesting high risk of tumorigenicity as using these cells for transplantation. Recently, Chiou et al. (<xref ref-type="bibr" rid="CR13">2013</xref>) reported that poly (ADP-ribose) polymerase 1 (Parp1) could be used for iPSC production, and it significantly decreases the risk of tumorigenicity, implying the major drawback could be overcome. However, the risk of teratoma formation after iPSCs transplantation could not be completely eliminated (Petit et al. <xref ref-type="bibr" rid="CR74">2014</xref>). Despite the obvious potential of iPSCs for cell-based therapy, this major hurdle should still be overcome before clinical use can be attempted.</p></sec><sec id="Sec5"><title>Neural stem cells (NSCs)</title><p>NSCs are stem-like progenitor cells that are isolated from either fetal brains or specific regions in adult brains (Kelly et al. <xref ref-type="bibr" rid="CR39">2004</xref>; Kukekov et al. <xref ref-type="bibr" rid="CR44">1999</xref>). In adult tissue, the subgranular zone (SGZ) in the dentate gyrus of the hippocampus and the subventricular zone (SVZ) of the lateral ventricles are two restricted regions producing NSCs, and these two regions confer neurogenesis in adult brain (Ming and Song <xref ref-type="bibr" rid="CR63">2011</xref>). NSCs are multipotent stem cells and recapitulate the developmental restriction toward a neural lineage. Therefore, these cells could be differentiated into neurons, astrocytes and oligodendrocytes (Jiang et al. <xref ref-type="bibr" rid="CR35">2012</xref>). Due to this specific lineage restriction, the risk of tumor formation is reduced, and NSCs are more easily guided toward neuronal differentiation. However, these cells cannot be isolated in large numbers, and it is also challenging to maintain or expand the cells in vitro over long periods of time (Anderson et al. <xref ref-type="bibr" rid="CR2">2007</xref>). As a result, the application of NSCs for transplantation is still limited.</p></sec><sec id="Sec6"><title>Mesenchymal stem cells (MSCs)</title><p>Mesenchymal stem cells are non-hematopoietic and multipotent cells first retrieved from the stromal area of the adult bone marrow (Fridenshtein <xref ref-type="bibr" rid="CR23">1991</xref>). In addition to bone marrow, MSCs may also be derived from a variety of non-marrow tissues, including placenta, muscle, skin, dental pulp, adipose tissue, umbilical cord and amniotic fluid (Jiang et al. <xref ref-type="bibr" rid="CR35">2012</xref>; Minguell et al. <xref ref-type="bibr" rid="CR64">2001</xref>). Since they can be retrieved from adult tissues, ethical concerns for MSCs could be avoided. Furthermore, one unique property of MSCs is immunomodulation, which may allow the cells to escape the surveillance of the host’s immune system or reduce the immune response of hosts (Guo et al. <xref ref-type="bibr" rid="CR29">2014</xref>; Glenn and Whartenby <xref ref-type="bibr" rid="CR26">2014</xref>). This characteristic would be an important concern for use in transplantation.</p><sec id="Sec600"><title>Bone marrow MSCs (BMSCs)</title><p>Bone marrow is the most common tissue from which MSCs are derived. The advantage of BMSCs is that these cells are relatively easy to be collected from patients’ own bone marrow without further CNS damage. Therefore, BMSCs may provide a relatively safe, ethical and immunologically favorable source for transplantation. In addition, application of BMSCs for the treatment of hematopoietic diseases began decades ago, which suggests that the protocol of isolation has been well established. As a result, BMSCs are considered as a resource with easier access. Another important feature is that BMSCs are able to cross the blood brain barrier and migrate throughout the brain (Li et al. <xref ref-type="bibr" rid="CR46">2001</xref>). This important advantage suggests the possibility that reconstruction/replacement of damaged brain tissues may be initiated via peripheral delivery without invasive methods. Furthermore, several reports have shown that BMSCs could be differentiated into neuronal cells (Zhao et al. <xref ref-type="bibr" rid="CR105">2015</xref>; Haragopal et al. <xref ref-type="bibr" rid="CR30">2015</xref>). These results support the therapeutic potential of BMSCs for neurological disease. However, the efficiency of differentiation into neuronal cells is low, and these cells may only be maintained for a few passages (Long et al. <xref ref-type="bibr" rid="CR53">2005</xref>). These drawbacks limit the potential application of BMSCs for transplantation.</p></sec><sec id="Sec1000"><title>Umbilical cord blood (UCB) cells</title><p>UCB is collected from the umbilical cord attached to the placenta during birth. UCB is comprised of hematopoietic stem cells, endothelial cell precursors, mesenchymal progenitors and multipotent/pluripotent lineage stem cells (Berger et al. <xref ref-type="bibr" rid="CR6">2006</xref>; Erices et al. <xref ref-type="bibr" rid="CR19">2000</xref>). Since these materials are considered to be waste products, UCB cells may be easily procured without damage to donors, thereby circumventing ethical issues. Another important characteristic of UCB cells is that they are more juvenile than those collected from adult tissues; therefore, these cells are easier to expand in culture, more tolerant to human leukocyte antigen (HLA) disparities, and significantly lower risk for immune rejection (Danby and Rocha <xref ref-type="bibr" rid="CR16">2014</xref>). The neurological pluripotency of UCB cells has been studied in several reports. Jang et al. showed that cord-derived hematopoietic stem cells could be differentiated into neuronal and glial cells (astrocytes and oligodendrocytes) using retinoic acid (Jang et al. <xref ref-type="bibr" rid="CR33">2004</xref>). Similarly, non-hematopoietic stem cells in UCB (most likely mesenchymal progenitors) also process the capability to differentiate into neural-like cells in vitro (Buzanska et al. <xref ref-type="bibr" rid="CR11">2006</xref>). Although the pluripotency of UCB toward neuronal lineage is beneficial for transplantation, the limited amount of cells which could be collected remains the main drawback for the utilization of UCB. Because of the restricted volume of cells collected from cord blood, the amount of stem cells in UCB is 10-fold less than that of bone marrow. As a result, UCB cells only are applicable in children or young adults (Moise <xref ref-type="bibr" rid="CR65">2005</xref>). Several strategies have been proposed to overcome this problem. For example, transplantations with double unit cord blood and ex vivo expansion of UCB cells have proved to offer better outcomes (Brunstein et al. <xref ref-type="bibr" rid="CR10">2009</xref>; Yoshimi et al. <xref ref-type="bibr" rid="CR102">2008</xref>). Therefore, UCB cells are still considered as one of potential resources for transplantation.</p></sec></sec></sec><sec id="Sec7"><title>Application of stem cells in Parkinson’s disease</title><sec id="Sec8"><title>Parkinson’s disease</title><p>Parkinson’s disease (PD) is the second most common neurodegenerative disorder, affecting 1 % of the population worldwide after the age of 65. The typical symptoms of PD are bradykinesia, rigidity, and resting tremor (Tanner and Goldman <xref ref-type="bibr" rid="CR89">1996</xref>). The main pathological features are extensive loss of dopamine (DA) neurons in the Substantia Nigra pars compacta and the accumulations of cytoplasmic eosinophilic inclusions, Lewy bodies (LB) (Forno <xref ref-type="bibr" rid="CR20">1996</xref>). The cause of degenerated nigrostriatal dopaminergic neurons remains largely unknown. Current therapeutic choices for PD patients include levodopa, DA agonists, monoamine oxidase inhibitors, and deep brain stimulation (DBS). Generally, the effectiveness of oral medications begins to wear-off after 5 years (Jankovic <xref ref-type="bibr" rid="CR34">2005</xref>). Moreover, these treatments cannot repair the damaged DAstriatal projections; therefore, restorative approaches should be considered in order to improve the therapeutic effect. Since PD patients display selective degeneration of SN DA neurons, cell replacement therapies which can produce functional DA neurons may be a valuable therapeutic approach.</p><p>To achieve a successful cell-based therapy in PD, some criteria for cell transplantation are generally suggested (Lindvall and Hagell <xref ref-type="bibr" rid="CR49">2000</xref>; Lindvall and Kokaia <xref ref-type="bibr" rid="CR50">2006</xref>; Lindvall et al. <xref ref-type="bibr" rid="CR52">2004</xref>). (1) The cells should possess the molecular, morphological and electrophysiological properties of DA neurons in substantia nigra; (2) the grafts should be able to reverse the motor deficits of PD; (3) the therapy should enable 100,000 or more DA neurons to survive long term in human putamen; (4) the grafted cells should re-establish a dense terminal network throughout the striatum to functionally integrate into host neural circuitries. Here we review the progress of stem cell therapies and discuss the major problems encountered in PD.</p></sec><sec id="Sec9"><title>Graft</title><p>The content of graft is the critical issue when performing the transplantation. It is currently unknown whether symptomatic relief would be best achieved by implanting a pure population of DA neurons or a graft containing a portion of glial cells. Several studies support the necessary role of astrocytes for neural differentiation during embryonic development, implying that glial cells are important for fate determination of precursors during implantation (Song et al. <xref ref-type="bibr" rid="CR84">2002</xref>). Therefore, mesencephalic tissues containing glial cells were most often used in previous studies. Another key issue in performing grafts for PD treatment is that implanting the most suitable subtype of DA neurons is also critical for the outcome of transplantation. DA rich-ventral mesencephalic grafts contain two types of DA neuron progenitors, including A9 Substantia Nigra neurons and A10 dopamine neurons of the Ventral Tegmental Area (Thompson et al. <xref ref-type="bibr" rid="CR90">2005</xref>). Only the A9 subtype DA neurons send innervated axons into the striatum in rats (O’Keeffe et al. <xref ref-type="bibr" rid="CR68">2008</xref>; Grealish et al. <xref ref-type="bibr" rid="CR28">2010</xref>), suggesting that mesencephalic grafts with more A9 subtype DA neurons would be more beneficial for PD treatment.</p><p>In late 1980s, clinicians transplanted human embryonic or fetal ventral mesencephalic tissues into PD patients, but the results were varied. In Madrazo and Lindvall’s open-label trials, PD patients showed improvement of Unified Parkinson’s Disease Rating Scale (UPDRS) after receiving fetal DA neuron graft (Madrazo et al. <xref ref-type="bibr" rid="CR58">1988</xref>; Lindvall et al. <xref ref-type="bibr" rid="CR51">1989</xref>). However, the results from two double-blind trials funded by the National Institutes of Health (NIH) in the 1990s showed no significant effects (Freed et al. <xref ref-type="bibr" rid="CR22">2001</xref>; Olanow et al. <xref ref-type="bibr" rid="CR69">2003</xref>). Even more, several side-effects have been shown in PD patients who received these transplantations. The results of these two open-label and double-blind trials raise critical issues regarding ethical considerations, and may enhance controversy which can dissuade the potential use of transplants for PD.</p><p>In the following, we will review different alternative sources for the transplantation in PD.</p><sec id="Sec2000"><title>ES cell-derived DA neurons</title><p>ES cells are one important source that has been used to differentiate into DA neurons in the laboratory. Rodent and human ES cell-derived DA neurons have been shown to survive and function after transplantation into the striatum of PD rats (Kim et al. <xref ref-type="bibr" rid="CR40">2002</xref>; Yang et al. <xref ref-type="bibr" rid="CR100">2008</xref>). In 2005, Takagi et al. reported that primate ES cell-derived DA neurons survived in the putamen of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP)-lesioned monkeys. Furthermore, the uptake of [<sup>18</sup>F]-DOPA also increased 14 weeks after transplantation, suggesting exogenous ES cell-derived DA neurons could offer the functional recovery of DA neurons. Until now, ES cells are still the most promising source to differentiate into DA neurons (Kim et al. <xref ref-type="bibr" rid="CR40">2002</xref>; Rodriguez-Gomez et al. <xref ref-type="bibr" rid="CR81">2007</xref>); however, the efficiency to differentiate into DA neurons and the survival rate of these neurons after transplantation are still low. For example, prior reports showed less than 300 tyrosine hydroxylase (TH)-positive neurons survived after transplanting 100,000–400,000 ES cells into the striatum (Brederlau et al. <xref ref-type="bibr" rid="CR9">2006</xref>; Ben-Hur et al. <xref ref-type="bibr" rid="CR5">2004</xref>). Therefore a critical issue that must be resolved to enhance recovery after transplantation in PD is improvement of the differentiation and survival rate.</p></sec><sec id="Sec3000"><title>iPSC-derived DA neurons</title><p>Since the iPSC technique was established in 2006 (Takahashi and Yamanaka <xref ref-type="bibr" rid="CR86">2006</xref>), another cell source to generate DA neurons was provided. In 2008, DA neurons were first generated from mouse iPSCs and transplanted into the striatum of a rat PD model, thereby alleviating the symptoms of PD (Wernig et al. <xref ref-type="bibr" rid="CR97">2008</xref>). In 2010, DA neurons differentiated from iPSCs of PD patients were transplanted into PD transgenic rats, and these neurons survived for several months and further alleviated the symptoms of PD (Hargus et al. <xref ref-type="bibr" rid="CR31">2010</xref>). Most importantly, these transplanted cells did not display α-synuclein positive inclusion bodies in hosts, suggesting that performing autografts in PD patients may be a viable option. However, several reports have mentioned patient-derived iPSCs are still more vulnerable to PD because of mutations or epigenetic markers in cells (Badger et al. <xref ref-type="bibr" rid="CR3">2014</xref>; Beevers et al. <xref ref-type="bibr" rid="CR4">2013</xref>; Sanchez-Danes et al. <xref ref-type="bibr" rid="CR82">2012</xref>). Furthermore, the risk of tumor formation still needs to be minimized before clinical application can be realized (Petit et al. <xref ref-type="bibr" rid="CR74">2014</xref>). Since the technique of iPSC production was only developed a few years ago, further optimization may overcome these drawbacks.</p></sec><sec id="Sec4000"><title>NSCs and NSC-derived DA neurons</title><p>NSCs are multipotent stem cells that are defined as “neurally” destined cells and retain their regional specificity (Horiguchi et al. <xref ref-type="bibr" rid="CR32">2004</xref>). Therefore, NSCs that are derived from a primarily DA location, such as ventral mesencephalon (VM), should be the most appropriate source of DA neurons. Several reports have shown the potential ability of NSCs to differentiate into DA neurons (Tan et al. <xref ref-type="bibr" rid="CR87">2014</xref>, <xref ref-type="bibr" rid="CR88">2015</xref>), and also demonstrated the improvement of symptoms in PD models after transplantation of NSC-derived DA neurons (Parish et al. <xref ref-type="bibr" rid="CR70">2008</xref>; Redmond et al. <xref ref-type="bibr" rid="CR79">2007</xref>). Additionally, overexpression of different genes, such as Lmx1a, glial cell line-derived neurotrophic factor (GDNF), Brn4 and TH, in NSCs has enhanced the beneficial effects of NSC-derived DA neurons (Tan et al. <xref ref-type="bibr" rid="CR87">2014</xref>; Wu et al. <xref ref-type="bibr" rid="CR99">2015</xref>; Wakeman et al. <xref ref-type="bibr" rid="CR95">2014</xref>). In animal studies, NSC-derived DA neurons overexpressing Nurr1, a critical factor involved in DA specification and survival, has led to functional improvement in rats treated with 6-hydroxydopamine (6-OHDA), a toxic-induced PD model (Park et al. <xref ref-type="bibr" rid="CR71">2006</xref>). However, the survival rate of TH positive neurons after transplantation was less than 4.3 % (Park et al. <xref ref-type="bibr" rid="CR71">2006</xref>; Studer et al. <xref ref-type="bibr" rid="CR85">1998</xref>). In 2008, Parish et al. transfected Wnt5a into NSCs from mouse VM, generating tenfold more DA neurons with TH positive signal than the conventional FGF2-treated NSCs from VM and causing functional recovery in 6-OHDA mice (Parish et al. <xref ref-type="bibr" rid="CR70">2008</xref>). Aside from VM, researchers have also derived NSCs from the SVZ, which is another well-known source for these cells. The transplantation of NSCs from SVZ enhanced the recovery of PD symptoms, but the survival rate of these cells was still low (Meissner et al. <xref ref-type="bibr" rid="CR60">2005</xref>; Richardson et al. <xref ref-type="bibr" rid="CR80">2005</xref>). Therefore, the most important issue that must be overcome in order to achieve NSC transplantation is to increase the cell number and survival rate of transplanted cells.</p></sec><sec id="Sec5000"><title>MSCs</title><p>Unlike studies using other stem cells, MSCs were grafted into PD models without differentiation in vitro in most studies; however, the spontaneous differentiation ability of BMSCs after transplantation is low (Mezey et al. <xref ref-type="bibr" rid="CR62">2000</xref>). Li et al. bilaterally injected BMSCs into striatum of MPTP-lesioned mice, and these cells showed TH immunoreactivity and promoted motor recovery (Li et al. <xref ref-type="bibr" rid="CR47">2001</xref>). However, only 0.8 % of implanted cells expressed TH immunoreactivity. To address the low differentiation rate, delivery of Notch1 intracellular domain (NICD), basic fibroblast growth factor (bFGF), forskolin, ciliary neurotrophic factor (CNTF) and GDNF has been used to efficiently induce BMSC differentiation into neuronal cells and increase the proportion of TH-positive cells (Dezawa et al. <xref ref-type="bibr" rid="CR18">2004</xref>). Moreover, the transplantation of these treated cells into 6-OHDA rats prevented DA neurons from degeneration (Glavaski-Joksimovic et al. <xref ref-type="bibr" rid="CR25">2009</xref>). Most importantly, in a clinical trial using BMSCs treated with bFGF, workers transplanted cells unilaterally into the ventricular zone of advanced PD patients, who showed modest clinical improvement at 12 months and no tumor formation (Venkataramana et al. <xref ref-type="bibr" rid="CR93">2010</xref>). This result suggests that BMSCs may be a good choice concerning the issue of safety.</p><p>MSCs isolated from umbilical cords have also shown beneficial effects in 6-OHDA PD models (Mathieu et al. <xref ref-type="bibr" rid="CR59">2012</xref>; Weiss et al. <xref ref-type="bibr" rid="CR96">2006</xref>). However, the low differentiation potential of UCB cells is similar to that of BMSCs. To improve the differentiation rate, UCB cells were cultured with sonic hedgehog and fibroblast growth factor-8 (FGF-8). Cells treated in this manner could reach 12.7 % neuronal differentiation, and these cells successfully ameliorated apomorphine-induced rotations in 6-OHDA lesioned rats (Fu et al. <xref ref-type="bibr" rid="CR24">2006</xref>). Overall, transplantation of undifferentiated MSCs or differentiated UCBs could all improve the symptoms of PD. Since there is no report to compare the difference between these cells, further studies will be necessary to conclude which source would be preferable.</p><p>In summary, iPSCs, NSCs, and MSCs are the most likely sources of stem cells for PD therapy. In all cases, autografts may be used as demonstrated by several successes in rodent and primate PD models. However, the diverse differentiation methods, low production rate, and low survival rate after transplantation are still obstacles that need to be overcome before clinical use.</p></sec></sec><sec id="Sec10"><title>Patient selection</title><p>The status of PD patients is a critical factor affecting the outcome after transplantation. Though prior clinical studies have reported diverse effects of transplantation in PD patients (Madrazo et al. <xref ref-type="bibr" rid="CR58">1988</xref>; Lindvall et al. <xref ref-type="bibr" rid="CR51">1989</xref>; Freed et al. <xref ref-type="bibr" rid="CR22">2001</xref>; Olanow et al. <xref ref-type="bibr" rid="CR69">2003</xref>), there are some conclusions that may be drawn from detailed analysis. Piccini et al. implanted embryonic ventral mesencephalic tissues into putamen or caudate of nine patients, and [<sup>18</sup>F]-DOPA PET was performed preoperatively and 1 or 2 years post-operatively. According to their results, patients without dopaminergic denervation outside the grafted striatal areas showed the best functional outcome after transplantation (Piccini et al. <xref ref-type="bibr" rid="CR76">2005</xref>). In Olanow’s trial, less severe patients (UPDRS <50 points during “off” medication) responded significantly better to fetal grafts (Olanow et al. <xref ref-type="bibr" rid="CR69">2003</xref>). Freed and coworkers suggested that patients with younger age or better levodopa response before surgery might benefit more from cell transplantation (Freed et al. <xref ref-type="bibr" rid="CR22">2001</xref>). Ma et al. used [<sup>18</sup>F]-DOPA PET to evaluate the outcome of 33 participants 2–4 years after transplantation and also found that younger recipients had better clinical improvement (Ma et al. <xref ref-type="bibr" rid="CR57">2010</xref>). In summary, individuals who are young and have better preoperative levodopa responsiveness will be more suitable for cell transplantation. In addition, patients with DA neurons loss restricted to the caudate-putamen will also receive more symptomatic benefit after transplantation.</p></sec><sec id="Sec11"><title>Immune response</title><p>Although the brain is regarded as an immune-privileged site, the host immune system still responds to the grafts. The interaction between implantation and the endogenous immune system affects the survival of grafted cells. In several clinical trials, transplantation without adequate immunosuppression may have led to poor outcomes (Freed et al. <xref ref-type="bibr" rid="CR22">2001</xref>; Olanow et al. <xref ref-type="bibr" rid="CR69">2003</xref>), while transplantation with an immunosuppressant, such as cyclosporine, azathioprine and prednisolone, produced better effects (Lindvall et al. <xref ref-type="bibr" rid="CR51">1989</xref>). Unfortunately, patient symptoms deteriorated after withdrawal of immunosuppression, and autopsy showed grafts were surrounded by activated microglia and immune reactivity (Olanow et al. <xref ref-type="bibr" rid="CR69">2003</xref>). These results imply that immune reactions exert a negative effect during transplantation, and it would be necessary to use an immunosuppressant in combination with grafting; however, further studies are still needed to determine the optimal immunosuppressant and the duration of treatment.</p></sec><sec id="Sec12"><title>Major issues after grafts</title><p>According to the reports of several cell-based studies in both animals and humans, there are two major concerns related to grafts.</p><sec id="Sec6000"><title>Graft Induced Dyskinesia (GID)</title><p>The occurrence of dyskinesia after transplantation was first reported by Defer et al. (<xref ref-type="bibr" rid="CR17">1996</xref>), but did not receive much attention until Freed’s trial in 2001 (Freed et al. <xref ref-type="bibr" rid="CR22">2001</xref>). They described the development of “graft induced dyskinesia (GID)” in 15 % of transplanted patients 1 year after transplantation. This unexpected symptom reached 56 % in Olanow’s study (Olanow et al. <xref ref-type="bibr" rid="CR69">2003</xref>). It is speculated that the number of grafted cells used in the surgery-controlled clinical trials was less than those of other more successful studies (Lindvall et al. <xref ref-type="bibr" rid="CR51">1989</xref>; Freed et al. <xref ref-type="bibr" rid="CR22">2001</xref>). Additionally, immunosuppression may be also an important factor since dyskinesia did not develop until immunosuppression withdrawal in several reports (Olanow et al. <xref ref-type="bibr" rid="CR69">2003</xref>; Piccini et al. <xref ref-type="bibr" rid="CR76">2005</xref>; Lane et al. <xref ref-type="bibr" rid="CR45">2008</xref>). The other possible issue is that heterogeneous grafts were found in ventral putamen, containing serotonergic neurons. These grafts led to islands of reinnervation and abnormal production of DA (Ma et al. <xref ref-type="bibr" rid="CR56">2002</xref>; Carlsson et al. <xref ref-type="bibr" rid="CR12">2009</xref>). Therefore, transplanting sufficient number of cells containing a pure population of DA neurons in basal ganglion with immunosuppression is suggested to avoid the development of GID.</p></sec><sec id="Sec7000"><title>Grafts affected by PD process</title><p>Evidence that PD pathology may propagate from host to grafts is emerging (Kordower et al. <xref ref-type="bibr" rid="CR42">2008a</xref>, <xref ref-type="bibr" rid="CR43">b</xref>; Li et al. <xref ref-type="bibr" rid="CR48">2008</xref>). The presence of LBs and Lewy neurites in grafted DA neurons were generally observed 11–16 years after human fetal mesencephalic transplantation (Kordower et al. <xref ref-type="bibr" rid="CR42">2008a</xref>, <xref ref-type="bibr" rid="CR43">b</xref>; Li et al. <xref ref-type="bibr" rid="CR48">2008</xref>; however,α-synuclein staining is generally not detectable in adults younger than 20 year-old (Chu and Kordower <xref ref-type="bibr" rid="CR14">2010</xref>). These observations imply that PD pathology can be transferred from host to graft (Visanji et al. <xref ref-type="bibr" rid="CR94">2013</xref>). The exact reasons for this negative outcome remain unresolved. A recent report showed that fetal cell transplantation in two PD patients remains highly functional even 15–18 years after surgery (Kefalopoulou et al. <xref ref-type="bibr" rid="CR38">2014</xref>). Therefore, although the spread of PD pathology may occur after transplantation, the period of beneficial effects from transplantation is still longer than that of current medications, suggesting stem cells still could be a potential clinical therapy.</p></sec></sec><sec id="Sec13"><title>Mechanisms of stem cell therapy in PD</title><p>From the positive results of prior studies, the effects of stem cell therapy on PD can be classified into two categories. The first is a direct repair pathway, which includes augmenting endogenous neurogenesis, DA neuron differentiation (Park et al. <xref ref-type="bibr" rid="CR72">2012</xref>), DA release (Rodriguez-Gomez et al. <xref ref-type="bibr" rid="CR81">2007</xref>; Bouchez et al. <xref ref-type="bibr" rid="CR8">2008</xref>), striatum reinnervation (Kordower et al. <xref ref-type="bibr" rid="CR41">1995</xref>) and neural circuits integration (Piccini et al. <xref ref-type="bibr" rid="CR75">2000</xref>; Bjorklund et al. <xref ref-type="bibr" rid="CR7">2002</xref>). The second is indirect repair system through trophic factors. Stem cells express various neurotrophic factors, such as brain derived neurotrophic factor (BDNF), nerve growth factor (NGF), cerebral dopamine neurotrophic factor (CDNF) or glial-derived neurotrophic factor (GDNF), and facilitate DA neuronal differentiation and maintenance. These bystander effects are especially likely to result from grafts comprised of NSCs and MSCs (Rafuse et al. <xref ref-type="bibr" rid="CR77">2005</xref>; Tolar et al. <xref ref-type="bibr" rid="CR92">2010</xref>; Yasuhara et al. <xref ref-type="bibr" rid="CR101">2006</xref>; Lu et al. <xref ref-type="bibr" rid="CR54">2003</xref>). However, it is still hard to distinguish clearly which pathway plays a dominant role, and, as a result, it is generally assumed that both direct and indirect pathways contribute to the beneficial effects after transplantation.</p></sec></sec><sec id="Sec14" sec-type="conclusion"><title>Conclusion</title><p>There is still no cure for PD since the precise mechanisms of this disease are largely unknown. High expectations have been placed on stem cell therapy to achieve this goal since many of the cell-based studies on PD animal models have shown positive results; however, the outcomes in clinical trials have not been consistent or convincing. This is possibly due to a combination of factors, such as patient selection, amount and mode of tissue engraftment and the level of immunosuppression. Additionally, another side effect to be considered is GID. Fortunately, grafted tissues were not affected by PD progression within 10 years after transplantation, so the treatment of PD with stem cell grafts is still a promising direction. The major advantage of this strategy is the restorative and trophic abilities of the grafted cells which reach far beyond drugs prescribed in current practice.</p></sec></body><back><fn-group><fn><p>Mu-Hui Fu, Chia-Ling Li and Hsiu-Lien Lin contributed equally to this work</p></fn></fn-group><ack><title>Authors’ contributions</title><p>MHF, CLL, HLL, PCC, MJC, YFC, PHC and SHY collected references, and MHF, CCL, HLL, PCC, MJC and SHY drafted the paper. All authors read and approved the final manuscript.</p><sec id="FPar1"><title>Acknowledgements</title><p>This work was supported by Ministry of Science and Technology (MOST 102-2628-B-006-010-MY3 and MOST 103-2320-B-006 -010) and, in part, the Ministry of Education, Taiwan, R.O.C. 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