A Review on Stem Cell Therapy for Neuropathic Pain

Author(s): Samira Asgharzade, Andisheh Talaei, Tahereh Farkhondeh, Fatemeh Forouzanfar*

Journal Name: Current Stem Cell Research & Therapy

Volume 15 , Issue 4 , 2020

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Abstract:

Neuropathic pain is a complex, chronic pain state that is heterogeneous in nature and caused by the consequence of a lesion or disease affecting the somatosensory system. Current medications give a long-lasting pain relief only in a limited percentage of patients also associated with numerous side effects. Stem cell transplantation is one of the attractive therapeutic platforms for the treatment of a variety of diseases, such as neuropathic pain. Here, the authors review the therapeutic effects of stem cell transplantation of different origin and species in different models of neuropathic pain disorders. Stem cell transplantation could alleviate the neuropathic pain; indeed, stem cells are the source of cells, which differentiate into a variety of cell types and lead trophic factors to migrate to the lesion site opposing the effects of damage. In conclusion, this review suggests that stem cell therapy can be a novel approach for the treatment of neuropathic pain.

Keywords: Stem cell therapy, chronic pain, neuropathic pain, mesenchymal stem cells, pain management, neurotrophic factor.

[1]
Mathew PJ, Mathew JL. Assessment and management of pain in infants. Postgrad Med J 2003; 79(934): 438-43.
[http://dx.doi.org/10.1136/pmj.79.934.438] [PMID: 12954954]
[2]
Vaughan S, Poole H, Forshaw M, et al. Pain Processing in Psychiatric Conditions. Syst Rev 2019; 23(3): 336-58.
[3]
Machelska H. Control of neuropathic pain by immune cells and opioids. CNS & Neurological Disorders-Drug Targets (Formerly Current Drug Targets-CNS & Neurological Disorders) 2 2011; 10(5): 559-70.
[http://dx.doi.org/10.2174/187152711796234952]
[4]
Lumley MA, Cohen JL, Borszcz GS, et al. Pain and emotion: a biopsychosocial review of recent research. J Clin Psychol 2011; 67(9): 942-68.
[http://dx.doi.org/10.1002/jclp.20816] [PMID: 21647882]
[5]
O’connell NE, Marston L, Spencer S, DeSouza LH, Wand BM. Non‐invasive brain stimulation techniques for chronic pain. Cochrane Sys Rev 2018.(3):
[6]
Treede R-D, Rief W, Barke A, et al. Chronic pain as a symptom or a disease: the IASP Classification of Chronic Pain for the International Classification of Diseases (ICD-11). Pain 2019; 160(1): 19-27.
[http://dx.doi.org/10.1097/j.pain.0000000000001384] [PMID: 30586067]
[7]
Jensen TS, Baron R, Haanpää M, et al. A new definition of neuropathic pain. Pain 2011; 152(10): 2204-5.
[http://dx.doi.org/10.1016/j.pain.2011.06.017] [PMID: 21764514]
[8]
Scholz J, Finnerup NB, Attal N, et al. The IASP classification of chronic pain for ICD-11: chronic neuropathic pain. Pain 2019; 160(1): 53-9.
[http://dx.doi.org/10.1097/j.pain.0000000000001365] [PMID: 30586071]
[9]
Gilron I, Watson CPN, Cahill CM, Moulin DE. Neuropathic pain: a practical guide for the clinician. CMAJ 2006; 175(3): 265-75.
[http://dx.doi.org/10.1503/cmaj.060146] [PMID: 16880448]
[10]
Mulla SM, Buckley DN, Moulin DE, et al. Management of chronic neuropathic pain: a protocol for a multiple treatment comparison meta-analysis of randomised controlled trials. BMJ Open 2014; 4(11): e006112
[http://dx.doi.org/10.1136/bmjopen-2014-006112] [PMID: 25412864]
[11]
Forouzanfar F, Hosseinzadeh H. Medicinal herbs in the treatment of neuropathic pain: a review. Iran J Basic Med Sci 2018; 21(4): 347-58.
[PMID: 29796216]
[12]
Seidel S, Aigner M, Wildner B, Sycha T, Pablik E. Antipsychotics for the treatment of neuropathic pain in adults. Cochrane Sys Rev 2018; (1):
[http://dx.doi.org/10.1002/14651858.CD012916]
[13]
Cohen SP, Mao J. Neuropathic pain: mechanisms and their clinical implications. BMJ 2014; 348: f7656.
[http://dx.doi.org/10.1136/bmj.f7656] [PMID: 24500412]
[14]
Attal N. Neuropathic pain: mechanisms, therapeutic approach, and interpretation of clinical trials. CONTINUUM: Lifelong Learning in Neurology 2012;
[http://dx.doi.org/10.1212/01.CON.0000411564.41709.2d]
[15]
Gilron I, Baron R, Jensen T, Eds. Neuropathic pain: principles of diagnosis and treatment Mayo Clinic Proceedings. Elsevier 2015.
[16]
Gao Y-J, Ji R-R. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther 2010; 126(1): 56-68.
[http://dx.doi.org/10.1016/j.pharmthera.2010.01.002] [PMID: 20117131]
[17]
Forouzanfar F, Hosseinzadeh H, Khorrami MB, Asgharzade S, Rakhshandeh H. Attenuating effect of Portulaca oleracea extract in chronic constriction injury induced neuropathic pain in rats: an evidence of anti-oxidative and anti-inflammatory properties. CNS Neurol Disord Drug Targets 2019.
[http://dx.doi.org/10.2174/1871527318666190314110528]
[18]
Zilliox LA. Neuropathic Pain. In:Continuum Minneapolis M Ed Selected Topics in Outpatient Neurology . 2017; 23: pp. 512-32.
[19]
Fornasari D. Pharmacotherapy for neuropathic pain: A review. Pain Ther 2017; 6(Suppl. 1): 25-33.
[http://dx.doi.org/10.1007/s40122-017-0091-4] [PMID: 29178034]
[20]
Derry S, Bell RF, Straube S, Wiffen PJ, Aldington D, Moore RA. Pregabalin for neuropathic pain in adults. Cochrane Sys Rev 2019. [Epub ahead of print]
[http://dx.doi.org/10.1002/14651858.CD007076.pub3]
[21]
Aiyer R, Mehta N, Gungor S, Gulati A. A systematic review of NMDA receptor antagonists for treatment of neuropathic pain in clinical practice. Clin J Pain 2018; 34(5): 450-67.
[PMID: 28877137]
[22]
Maienschein J. Regenerative medicine’s historical roots in regeneration, transplantation, and translation. Dev Biol 2011; 358(2): 278-84.
[http://dx.doi.org/10.1016/j.ydbio.2010.06.014] [PMID: 20561516]
[23]
Biehl JK, Russell B. Introduction to stem cell therapy. J Cardiovasc Nurs 2009; 24(2): 98-103.
[http://dx.doi.org/10.1097/JCN.0b013e318197a6a5] [PMID: 19242274]
[24]
Gazit Z, Pelled G, Sheyn D, Yakubovich DC, Gazit D. Mesenchymal stem cells Principles of regenerative medicine. Elsevier 2019; pp. 205-18.
[25]
Naderi-Meshkin H, Bahrami AR, Bidkhori HR, Mirahmadi M, Ahmadiankia N. Strategies to improve homing of mesenchymal stem cells for greater efficacy in stem cell therapy. Cell Biol Int 2015; 39(1): 23-34.
[http://dx.doi.org/10.1002/cbin.10378] [PMID: 25231104]
[26]
Abati E, Bresolin N, Comi GP, Corti S. Preconditioning and cellular engineering to increase the survival of transplanted neural stem cells for motor neuron disease therapy. Mol Neurobiol 2019; 56(5): 3356-67.
[http://dx.doi.org/10.1007/s12035-018-1305-4] [PMID: 30120734]
[27]
Strom SC, Jorns C. Cell therapy of liver disease: From hepatocytes to stem cells Principles of Regenerative Medicine. Elsevier 2019; pp. 229-46.
[http://dx.doi.org/10.1016/B978-0-12-809880-6.00016-3]
[28]
Kim SU, de Vellis J. Stem cell-based cell therapy in neurological diseases: a review. J Neurosci Res 2009; 87(10): 2183-200.
[http://dx.doi.org/10.1002/jnr.22054] [PMID: 19301431]
[29]
Park I-H, Zhao R, West JA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008; 451(7175): 141-6.
[http://dx.doi.org/10.1038/nature06534] [PMID: 18157115]
[30]
Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997; 276(5309): 71-4.
[http://dx.doi.org/10.1126/science.276.5309.71] [PMID: 9082988]
[31]
Fehrer C, Lepperdinger G. Mesenchymal stem cell aging. Exp Gerontol 2005; 40(12): 926-30.
[http://dx.doi.org/10.1016/j.exger.2005.07.006] [PMID: 16125890]
[32]
Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976; 4(5): 267-74.
[PMID: 976387]
[33]
Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2008; 2(4): 313-9.
[http://dx.doi.org/10.1016/j.stem.2008.03.002] [PMID: 18397751]
[34]
Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007; 25(11): 2739-49.
[http://dx.doi.org/10.1634/stemcells.2007-0197] [PMID: 17656645]
[35]
Klimczak A, Kozlowska U. Mesenchymal stromal cells and tissue-specific progenitor cells: Their role in tissue homeostasis. Stem Cells Int 2016; 2016: 4285215
[http://dx.doi.org/10.1155/2016/4285215]
[36]
Barry FP, Murphy JM. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 2004; 36(4): 568-84.
[http://dx.doi.org/10.1016/j.biocel.2003.11.001] [PMID: 15010324]
[37]
Baksh D, Song L, Tuan RS. Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 2004; 8(3): 301-16.
[http://dx.doi.org/10.1111/j.1582-4934.2004.tb00320.x] [PMID: 15491506]
[38]
Gao F, Chiu SM, Motan DA, et al. Mesenchymal stem cells and immunomodulation: current status and future prospects. Cell Death Dis 2016; 7(1): e2062
[http://dx.doi.org/10.1038/cddis.2015.327] [PMID: 26794657]
[39]
Zhao Q, Ren H, Han Z. Mesenchymal stem cells: Immunomodulatory capability and clinical potential in immune diseases. Journal of Cellular Immunotherapy 2016; 2(1): 3-20.
[http://dx.doi.org/10.1016/j.jocit.2014.12.001]
[40]
Mancuso P, Raman S, Glynn A, Barry F, Murphy JM. Mesenchymal Stem Cell Therapy for Osteoarthritis: The Critical Role of the Cell Secretome. Front Bioeng Biotechnol 2019; 7: 9.
[http://dx.doi.org/10.3389/fbioe.2019.00009] [PMID: 30761298]
[41]
Mazzini L, Mareschi K, Ferrero I, et al. Mesenchymal stromal cell transplantation in amyotrophic lateral sclerosis: a long-term safety study. Cytotherapy 2012; 14(1): 56-60.
[http://dx.doi.org/10.3109/14653249.2011.613929] [PMID: 21954839]
[42]
Hare JM, Traverse JH, Henry TD, et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009; 54(24): 2277-86.
[http://dx.doi.org/10.1016/j.jacc.2009.06.055] [PMID: 19958962]
[43]
Siniscalco D, Giordano C, Galderisi U, et al. Long-lasting effects of human mesenchymal stem cell systemic administration on pain-like behaviors, cellular, and biomolecular modifications in neuropathic mice. Front Integr Nuerosci 2011; 5: 79.
[http://dx.doi.org/10.3389/fnint.2011.00079] [PMID: 22164136]
[44]
Klass M, Gavrikov V, Drury D, et al. Intravenous mononuclear marrow cells reverse neuropathic pain from experimental mononeuropathy. Anesth Analg 2007; 104(4): 944-8.
[http://dx.doi.org/10.1213/01.ane.0000258021.03211.d0] [PMID: 17377111]
[45]
Yousefifard M, Nasirinezhad F, Shardi Manaheji H, Janzadeh A, Hosseini M, Keshavarz M. Human bone marrow-derived and umbilical cord-derived mesenchymal stem cells for alleviating neuropathic pain in a spinal cord injury model. Stem Cell Res Ther 2016; 7(1): 36.
[http://dx.doi.org/10.1186/s13287-016-0295-2] [PMID: 26957122]
[46]
Siniscalco D, Giordano C, Galderisi U, et al. Intra-brain microinjection of human mesenchymal stem cells decreases allodynia in neuropathic mice. Cell Mol Life Sci 2010; 67(4): 655-69.
[http://dx.doi.org/10.1007/s00018-009-0202-4] [PMID: 19937263]
[47]
Fischer G, Wang F, Xiang H, Bai X, Yu H, Hogan QH. Inhibition of neuropathic hyperalgesia by intrathecal bone marrow stromal cells is associated with alteration of multiple soluble factors in cerebrospinal fluid. Exp Brain Res 2017; 235(9): 2627-38.
[http://dx.doi.org/10.1007/s00221-017-5000-x] [PMID: 28573310]
[48]
Chen G, Park C-K, Xie R-G, Ji R-R. Intrathecal bone marrow stromal cells inhibit neuropathic pain via TGF-β secretion. J Clin Invest 2015; 125(8): 3226-40.
[http://dx.doi.org/10.1172/JCI80883] [PMID: 26168219]
[49]
Sun Y, Zhang D, Li H, Long R, Sun Q. Intrathecal administration of human bone marrow mesenchymal stem cells genetically modified with human proenkephalin gene decrease nociceptive pain in neuropathic rats. Mol Pain 2017; 13: 1744806917701445
[http://dx.doi.org/10.1177/1744806917701445] [PMID: 28326940]
[50]
Li J, Deng G, Wang H, et al. Interleukin-1β pre-treated bone marrow stromal cells alleviate neuropathic pain through CCL7-mediated inhibition of microglial activation in the spinal cord. Sci Rep 2017; 7: 42260.
[http://dx.doi.org/10.1038/srep42260] [PMID: 28195183]
[51]
Zhang EJ, Song CH, Ko YK, Lee WH. Intrathecal administration of mesenchymal stem cells reduces the reactive oxygen species and pain behavior in neuropathic rats. Korean J Pain 2014; 27(3): 239-45.
[http://dx.doi.org/10.3344/kjp.2014.27.3.239] [PMID: 25031809]
[52]
Schäfer S, Berger JV, Deumens R, Goursaud S, Hanisch UK, Hermans E. Influence of intrathecal delivery of bone marrow-derived mesenchymal stem cells on spinal inflammation and pain hypersensitivity in a rat model of peripheral nerve injury. J Neuroinflammation 2014; 11: 157.
[http://dx.doi.org/10.1186/s12974-014-0157-8] [PMID: 25212534]
[53]
Waterman RS, Tomchuck SL, Henkle SL, Betancourt AM. A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an Immunosuppressive MSC2 phenotype. PLoS One 2010; 5(4): e10088
[http://dx.doi.org/10.1371/journal.pone.0010088] [PMID: 20436665]
[54]
Waterman RS, Morgenweck J, Nossaman BD, Scandurro AE, Scandurro SA, Betancourt AM. Anti-inflammatory mesenchymal stem cells (MSC2) attenuate symptoms of painful diabetic peripheral neuropathy. Stem Cells Transl Med 2012; 1(7): 557-65.
[http://dx.doi.org/10.5966/sctm.2012-0025] [PMID: 23197860]
[55]
Shibata T, Naruse K, Kamiya H, et al. Transplantation of bone marrow-derived mesenchymal stem cells improves diabetic polyneuropathy in rats. Diabetes 2008; 57(11): 3099-107.
[http://dx.doi.org/10.2337/db08-0031] [PMID: 18728233]
[56]
Al-Massri KF, Ahmed LA, El-Abhar HS. Mesenchymal stem cells therapy enhances the efficacy of pregabalin and prevents its motor impairment in paclitaxel-induced neuropathy in rats: Role of Notch1 receptor and JAK/STAT signaling pathway. Behav Brain Res 2019; 360: 303-11.
[http://dx.doi.org/10.1016/j.bbr.2018.12.013] [PMID: 30543902]
[57]
Sacerdote P, Niada S, Franchi S, et al. Systemic administration of human adipose-derived stem cells reverts nociceptive hypersensitivity in an experimental model of neuropathy. Stem Cells Dev 2013; 22(8): 1252-63.
[http://dx.doi.org/10.1089/scd.2012.0398] [PMID: 23190263]
[58]
Forouzanfar F, Amin B, Ghorbani A, et al. New approach for the treatment of neuropathic pain: Fibroblast growth factor 1 gene-transfected adipose-derived mesenchymal stem cells. Eur J Pain 2018; 22(2): 295-310.
[http://dx.doi.org/10.1002/ejp.1119] [PMID: 28949091]
[59]
Mert T, Kurt AH, Altun İ, Celik A, Baran F, Gunay I. Pulsed magnetic field enhances therapeutic efficiency of mesenchymal stem cells in chronic neuropathic pain model. Bioelectromagnetics 2017; 38(4): 255-64.
[http://dx.doi.org/10.1002/bem.22038] [PMID: 28130880]
[60]
Lee HY, Lee HL, Yun Y, et al. Human Adipose Stem Cells Improve Mechanical Allodynia and Enhance Functional Recovery in a Rat Model of Neuropathic Pain. Tissue Eng Part A 2015; 21(13-14): 2044-52.
[http://dx.doi.org/10.1089/ten.tea.2014.0713] [PMID: 25857679]
[61]
Di Cesare Mannelli L, Tenci B, Micheli L, et al. Adipose-derived stem cells decrease pain in a rat model of oxaliplatin-induced neuropathy: Role of VEGF-A modulation. Neuropharmacology 2018; 131: 166-75.
[http://dx.doi.org/10.1016/j.neuropharm.2017.12.020] [PMID: 29241656]
[62]
Lin CH, Wu SH, Lee SS, et al. Autologous Adipose-Derived Stem Cells Reduce Burn-Induced Neuropathic Pain in a Rat Model. Int J Mol Sci 2017; 19(1): E34
[http://dx.doi.org/10.3390/ijms19010034] [PMID: 29271925]
[63]
Guimarães ET, Cruz GdaS, Almeida TF, et al. Transplantation of stem cells obtained from murine dental pulp improves pancreatic damage, renal function, and painful diabetic neuropathy in diabetic type 1 mouse model. Cell Transplant 2013; 22(12): 2345-54.
[http://dx.doi.org/10.3727/096368912X657972] [PMID: 23068779]
[64]
Datta I, Bhadri N, Shahani P, et al. Functional recovery upon human dental pulp stem cell transplantation in a diabetic neuropathy rat model. Cytotherapy 2017; 19(10): 1208-24.
[http://dx.doi.org/10.1016/j.jcyt.2017.07.009] [PMID: 28864291]
[65]
Shiue SJ, Rau RH, Shiue HS, et al. Mesenchymal stem cell exosomes as a cell-free therapy for nerve injury-induced pain in rats. Pain 2019; 160(1): 210-23.
[http://dx.doi.org/10.1097/j.pain.0000000000001395] [PMID: 30188455]
[66]
Lee MJ, Yoon TG, Kang M, Kim HJ, Kang KS. Effect of subcutaneous treatment with human umbilical cord blood-derived multipotent stem cells on peripheral neuropathic pain in rats. Korean J Physiol Pharmacol 2017; 21(2): 153-60.
[http://dx.doi.org/10.4196/kjpp.2017.21.2.153] [PMID: 28280408]
[67]
Chen C, Chen F, Yao C, et al. Intrathecal Injection of Human Umbilical Cord-Derived Mesenchymal Stem Cells Ameliorates Neuropathic Pain in Rats. Neurochem Res 2016; 41(12): 3250-60.
[http://dx.doi.org/10.1007/s11064-016-2051-5] [PMID: 27655256]
[68]
Chiang CY, Liu SA, Sheu ML, et al. Feasibility of Human Amniotic Fluid Derived Stem Cells in Alleviation of Neuropathic Pain in Chronic Constrictive Injury Nerve Model. PLoS One 2016; 11(7): e0159482
[http://dx.doi.org/10.1371/journal.pone.0159482] [PMID: 27441756]
[69]
Takagi Y. History of neural stem cell research and its clinical application. Neurol Med Chir (Tokyo) 2016; 56(3): 110-24.
[http://dx.doi.org/10.2176/nmc.ra.2015-0340] [PMID: 26888043]
[70]
Oikari L, Griffiths L, Haupt L. The current state of play in human neural stem cell models: what we have learnt from the rodent. OA Stem Cells 2014; 2(1): 7.
[71]
Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell 2015; 17(1): 11-22.
[http://dx.doi.org/10.1016/j.stem.2015.06.007] [PMID: 26140604]
[72]
Vogel A, Upadhya R, Shetty AK. Neural stem cell derived extracellular vesicles: Attributes and prospects for treating neurodegenerative disorders. EBioMedicine 2018; 38: 273-82.
[http://dx.doi.org/10.1016/j.ebiom.2018.11.026] [PMID: 30472088]
[73]
Götz M, Sirko S, Beckers J, Irmler M. Reactive astrocytes as neural stem or progenitor cells: In vivo lineage, In vitro potential, and Genome-wide expression analysis. Glia 2015; 63(8): 1452-68.
[http://dx.doi.org/10.1002/glia.22850] [PMID: 25965557]
[74]
Baker EW, Kinder HA, West FD. Neural stem cell therapy for stroke: A multimechanistic approach to restoring neurological function. Brain Behav 2019; 9(3): e01214
[http://dx.doi.org/10.1002/brb3.1214] [PMID: 30747485]
[75]
Lee HL, Oh J, Yun Y, et al. Vascular endothelial growth factor-expressing neural stem cell for the treatment of neuropathic pain. Neuroreport 2015; 26(7): 399-404.
[http://dx.doi.org/10.1097/WNR.0000000000000359] [PMID: 25793634]
[76]
Jergova S, Gajavelli S, Pathak N, Sagen J. Recombinant neural progenitor transplants in the spinal dorsal horn alleviate chronic central neuropathic pain. Pain 2016; 157(4): 977-89.
[http://dx.doi.org/10.1097/j.pain.0000000000000471] [PMID: 26761378]
[77]
Xu Q, Zhang M, Liu J, Li W. Intrathecal transplantation of neural stem cells appears to alleviate neuropathic pain in rats through release of GDNF. Ann Clin Lab Sci 2013; 43(2): 154-62.
[PMID: 23694790]
[78]
Du X-J, Chen Y-X, Zheng Z-C, Wang N, Wang X-Y, Kong F-E. Neural stem cell transplantation inhibits glial cell proliferation and P2X receptor-mediated neuropathic pain in spinal cord injury rats. Neural Regen Res 2019; 14(5): 876-85.
[http://dx.doi.org/10.4103/1673-5374.249236] [PMID: 30688274]
[79]
Franchi S, Valsecchi AE, Borsani E, et al. Intravenous neural stem cells abolish nociceptive hypersensitivity and trigger nerve regeneration in experimental neuropathy. Pain 2012; 153(4): 850-61.
[http://dx.doi.org/10.1016/j.pain.2012.01.008] [PMID: 22321918]
[80]
Baharvand H, Jafary H, Massumi M, Ashtiani SK. Generation of insulin-secreting cells from human embryonic stem cells. Dev Growth Differ 2006; 48(5): 323-32.
[http://dx.doi.org/10.1111/j.1440-169X.2006.00867.x] [PMID: 16759282]
[81]
Sundberg M, Andersson P-H, Åkesson E, et al. Markers of pluripotency and differentiation in human neural precursor cells derived from embryonic stem cells and CNS tissue. Cell Transplant 2011; 20(2): 177-91.
[http://dx.doi.org/10.3727/096368910X527266] [PMID: 20875224]
[82]
Pal R, Mamidi MK, Das AK, Bhonde R. Comparative analysis of cardiomyocyte differentiation from human embryonic stem cells under 3-D and 2-D culture conditions. J Biosci Bioeng 2013; 115(2): 200-6.
[http://dx.doi.org/10.1016/j.jbiosc.2012.08.018] [PMID: 23040993]
[83]
Miki T, Ring A, Gerlach J. Hepatic differentiation of human embryonic stem cells is promoted by three-dimensional dynamic perfusion culture conditions. Tissue Eng Part C Methods 2011; 17(5): 557-68.
[http://dx.doi.org/10.1089/ten.tec.2010.0437] [PMID: 21210720]
[84]
Löser P, Schirm J, Guhr A, Wobus AM, Kurtz A. Human embryonic stem cell lines and their use in international research. Stem Cells 2010; 28(2): 240-6.
[PMID: 20027651]
[85]
Meng G, Liu S, Li X, Krawetz R, Rancourt DE. Derivation of human embryonic stem cell lines after blastocyst microsurgery. Biochem Cell Biol 2010; 88(3): 479-90.
[http://dx.doi.org/10.1139/O09-188] [PMID: 20555390]
[86]
Ström S, Inzunza J, Grinnemo K-H, et al. Mechanical isolation of the inner cell mass is effective in derivation of new human embryonic stem cell lines. Hum Reprod 2007; 22(12): 3051-8.
[http://dx.doi.org/10.1093/humrep/dem335] [PMID: 17959612]
[87]
Khan FA, Almohazey D, Alomari M, Almofty SA. Isolation, Culture, and Functional Characterization of Human Embryonic Stem Cells: Current Trends and Challenges. Stem cells international 2018 2018.
[88]
Fandel TM, Trivedi A, Nicholas CR, et al. Transplanted Human Stem Cell-Derived Interneuron Precursors Mitigate Mouse Bladder Dysfunction and Central Neuropathic Pain after Spinal Cord Injury. Cell Stem Cell 2016; 19(4): 544-57.
[http://dx.doi.org/10.1016/j.stem.2016.08.020] [PMID: 27666009]
[89]
Hwang I, Hahm SC, Choi KA, et al. Intrathecal Transplantation of Embryonic Stem Cell-Derived Spinal GABAergic Neural Precursor Cells Attenuates Neuropathic Pain in a Spinal Cord Injury Rat Model. Cell Transplant 2016; 25(3): 593-607.
[http://dx.doi.org/10.3727/096368915X689460] [PMID: 26407027]
[90]
Ichim TE, Solano F, Lara F, et al. Feasibility of combination allogeneic stem cell therapy for spinal cord injury: a case report. Int Arch Med 2010; 3(1): 30.
[http://dx.doi.org/10.1186/1755-7682-3-30] [PMID: 21070647]
[91]
Venturi M, Boccasanta P, Lombardi B, Brambilla M, Contessini Avesani E, Vergani C. Pudendal neuralgia: A new option for treatment? Preliminary results on feasibility and efficacy. Pain Med 2015; 16(8): 1475-81.
[http://dx.doi.org/10.1111/pme.12693] [PMID: 25677417]
[92]
Vickers ER, Karsten E, Flood J, Lilischkis R. A preliminary report on stem cell therapy for neuropathic pain in humans. J Pain Res 2014; 7: 255-63.
[http://dx.doi.org/10.2147/JPR.S63361] [PMID: 24855388]
[93]
Squillaro T, Peluso G, Galderisi U. Clinical trials with mesenchymal stem cells: an update. Cell Transplant 2016; 25(5): 829-48.
[http://dx.doi.org/10.3727/096368915X689622] [PMID: 26423725]
[94]
Mousavinejad M, Andrews PW, Shoraki EK. Current biosafety considerations in stem cell therapy. Cell J 2016; 18(2): 281-7.
[PMID: 27540533]
[95]
Sasaki M, Abe R, Fujita Y, Ando S, Inokuma D, Shimizu H. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. Journal of immunology (Baltimore, Md : 1950) 2008; 180(4): 2581-7.
[http://dx.doi.org/10.4049/jimmunol.180.4.2581]
[96]
Liu H, Liu S, Li Y, et al. The role of SDF-1-CXCR4/CXCR7 axis in the therapeutic effects of hypoxia-preconditioned mesenchymal stem cells for renal ischemia/reperfusion injury. PLoS One 2012; 7(4): e34608
[http://dx.doi.org/10.1371/journal.pone.0034608] [PMID: 22511954]
[97]
Lee MJ, Kim J, Kim MY, et al. Proteomic analysis of tumor necrosis factor-α-induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res 2010; 9(4): 1754-62.
[http://dx.doi.org/10.1021/pr900898n] [PMID: 20184379]
[98]
Franchi S, Castelli M, Amodeo G, et al. Adult stem cell as new advanced therapy for experimental neuropathic pain treatment. BioMed Res Int 2014; 2014: 470983
[http://dx.doi.org/10.1155/2014/470983] [PMID: 25197647]
[99]
Chen L, Huang H, Sharma HS, Zuo H, Sanberg PR. Cell transplantation as a pain therapy targets both analgesia and neural repair. Cell Transplant 2013; 22(Suppl. 1): S11-9.
[http://dx.doi.org/10.3727/096368913X672091] [PMID: 23992823]
[100]
Koh S-H, Kim KS, Choi MR, et al. Implantation of human umbilical cord-derived mesenchymal stem cells as a neuroprotective therapy for ischemic stroke in rats. Brain Res 2008; 1229: 233-48.
[http://dx.doi.org/10.1016/j.brainres.2008.06.087] [PMID: 18634757]
[101]
Kwon S, Ki SM, Park SE, et al. Anti-apoptotic effects of human Wharton’s jelly-derived mesenchymal stem cells on skeletal muscle cells mediated via secretion of XCL1. Mol Ther 2016; 24(9): 1550-60.
[http://dx.doi.org/10.1038/mt.2016.125] [PMID: 27434589]
[102]
Lee RH, Yoon N, Reneau JC, Prockop DJ. Preactivation of human MSCs with TNF-α enhances tumor-suppressive activity. Cell Stem Cell 2012; 11(6): 825-35.
[http://dx.doi.org/10.1016/j.stem.2012.10.001] [PMID: 23142520]
[103]
Caplan AI, Correa D. The MSC: an injury drugstore. Cell Stem Cell 2011; 9(1): 11-5.
[http://dx.doi.org/10.1016/j.stem.2011.06.008] [PMID: 21726829]
[104]
Caplan AI, Hariri R. Body management: mesenchymal stem cells control the internal regenerator. Stem Cells Transl Med 2015; 4(7): 695-701.
[http://dx.doi.org/10.5966/sctm.2014-0291] [PMID: 26019227]
[105]
Akiyama Y, Radtke C, Honmou O, Kocsis JD. Remyelination of the spinal cord following intravenous delivery of bone marrow cells. Glia 2002; 39(3): 229-36.
[http://dx.doi.org/10.1002/glia.10102] [PMID: 12203389]
[106]
Satake K, Lou J, Lenke LG. Migration of mesenchymal stem cells through cerebrospinal fluid into injured spinal cord tissue. Spine 2004; 29(18): 1971-9.
[http://dx.doi.org/10.1097/01.brs.0000138273.02820.0a] [PMID: 15371697]
[107]
Yuan H, Ouyang S, Yang R, et al. Osthole alleviated diabetic neuropathic pain mediated by the P2X4 receptor in dorsal root ganglia. Brain Res Bull 2018; 142: 289-96.
[http://dx.doi.org/10.1016/j.brainresbull.2018.08.008] [PMID: 30118750]
[108]
Deng J, Zhang Y, Xie Y, Zhang L, Tang P. Cell transplantation for spinal cord injury: tumorigenicity of induced pluripotent stem cellderived neural stem/progenitor cells. Stem cells international 2018 2018.
[109]
Hosseini SM, Sani M, Haider KH, et al. Concomitant use of mesenchymal stem cells and neural stem cells for treatment of spinal cord injury: A combo cell therapy approach. Neurosci Lett 2018; 668: 138-46.
[http://dx.doi.org/10.1016/j.neulet.2018.01.008] [PMID: 29317311]
[110]
Mimeault M, Hauke R, Batra SK. Stem cells: a revolution in therapeutics-recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies. Clin Pharmacol Ther 2007; 82(3): 252-64.
[http://dx.doi.org/10.1038/sj.clpt.6100301] [PMID: 17671448]
[111]
Juengst E, Fossel M. The ethics of embryonic stem cells--now and forever, cells without end. JAMA 2000; 284(24): 3180-4.
[http://dx.doi.org/10.1001/jama.284.24.3180] [PMID: 11135785]
[112]
Baldwin T. Morality and human embryo research. Introduction to the Talking Point on morality and human embryo research. EMBO Rep 2009; 10(4): 299-300.
[http://dx.doi.org/10.1038/embor.2009.37] [PMID: 19337297]
[113]
Li J-Y, Christophersen NS, Hall V, Soulet D, Brundin P. Critical issues of clinical human embryonic stem cell therapy for brain repair. Trends Neurosci 2008; 31(3): 146-53.
[http://dx.doi.org/10.1016/j.tins.2007.12.001] [PMID: 18255164]


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VOLUME: 15
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Year: 2020
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DOI: 10.2174/1574888X15666200214112908
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