Bone marrow-derived mesenchymal stem cells improve diabetic neuropathy by direct modulation of both angiogenesis and myelination in peripheral nerves

Cell Transplantation

Volumn 25, Issue 2, 2016, Pages 313-326

  Han, Ji Woong ^a   Choi, Dabin ^a   Lee, Min Young ^a   Huh, Yang Hoon ^b   Yoon, Young Sup ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

Angiogenesis; Bone marrow; Diabetic neuropathy (DN); Mesenchymal stem cells (MSCs); Myelination

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; FIBROBLAST GROWTH FACTOR 2; GELATINASE A; GLUCOSE; MYELIN BASIC PROTEIN; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIC FACTOR; PROSTAGLANDIN F; PROTEIN S100B; STREPTOZOCIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CAPILLARY DENSITY; CELL ULTRASTRUCTURE; COCULTURE; CONTROLLED STUDY; DIABETIC NEUROPATHY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HINDLIMB MUSCLE; HISTOPATHOLOGY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOTOR NERVE CONDUCTION; MOUSE; MYELINATED NERVE; MYELINATION; NERVE REGENERATION; NEUROMODULATION; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCIATIC NERVE; SENSORY NERVE CONDUCTION VELOCITY; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; THERAPY EFFECT; UPREGULATION; ANIMAL; BONE MARROW; CELL CULTURE; CYTOLOGY; DIABETIC NEUROPATHIES; EXPERIMENTAL DIABETES MELLITUS; MESENCHYMAL STROMA CELL; METABOLISM; MYELIN SHEATH; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; PROCEDURES; SCHWANN CELL; WISTAR RAT;

ANIMALS; BONE MARROW; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MYELIN SHEATH; NEOVASCULARIZATION, PATHOLOGIC; NERVE REGENERATION; RATS, WISTAR; SCHWANN CELLS; SCIATIC NERVE;

EID: 84957069459     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368915X688209     Document Type: Article

References (57)

1. Ajroud-Driss, S.; Christiansen, M.; Allen, J. A.; Kessler, J. A. Phase 1/2 open-label dose-escalation study of plasmid DNA expressing two isoforms of hepatocyte growth factor in patients with painful diabetic peripheral neuropathy. Mol. Ther. 21(6):1279–1286; 2013.
2. Akiyama, Y.; Radtke, C.; Honmou, O.; Kocsis, J. D. Remyelination of the spinal cord following intravenous delivery of bone marrow cells. Glia 39(3):229–236; 2002.
3. Al-Khaldi, A.; Al-Sabti, H.; Galipeau, J.; Lachapelle, K. Therapeutic angiogenesis using autologous bone marrow stromal cells: Improved blood flow in a chronic limb ischemia model. Ann. Thorac. Surg. 75(1):204–209; 2003.
4. Anitha, M.; Gondha, C.; Sutliff, R.; Parsadanian, A.; Mwangi, S.; Sitaraman, S. V.; Srinivasan, S. Gdnf rescues hyperglycemia-induced diabetic enteric neuropathy through activation of the pi3k/akt pathway. J. Clin. Invest. 116(2):344–356; 2006.
5. Balsam, L. B.; Wagers, A. J.; Christensen, J. L.; Kofidis, T.; Weissman, I. L.; Robbins, R. C. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428(6983):668–673; 2004.
6. Britland, S. T.; Sharma, A. K.; Duguid, I. G.; Thomas, P. K. Ultrastructural observations on myelinated fibres in the tibial nerve of streptozotocin-diabetic rats: Effect of insulin treatment. Life Support Syst. 3(Suppl. 1):524–529; 1985.
7. Caddick, J.; Kingham, P. J.; Gardiner, N. J.; Wiberg, M.; Terenghi, G. Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54(8):840–849; 2006.
8. Cho, H. J.; Lee, N.; Lee, J. Y.; Choi, Y. J.; Ii, M.; Wecker, A.; Jeong, J. O.; Curry, C.; Qin, G.; Yoon, Y. S. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J. Exp. Med. 204(13):3257–3269; 2007.
9. Chong, M. S.; Hester, J. Diabetic painful neuropathy: Current and future treatment options. Drugs 67(4):569–585; 2007.
10. Eckersley, L. Role of the Schwann cell in diabetic neuropathy. Int. Rev. Neurobiol. 50:293–321; 2002.
11. Fazan, V. P.; Salgado, H. C.; Barreira, A. A. Aortic depressor nerve myelinated fibers in acute and chronic experimental diabetes. Am. J. Hypertens. 19(2):153–160; 2006.
12. Frostick, S. P.; Yin, Q.; Kemp, G. J. Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 18(7):397–405; 1998.
13. Gnecchi, M.; Danieli, P.; Cervio, E. Mesenchymal stem cell therapy for heart disease. Vascul. Pharmacol. 57(1):48–55; 2012.
14. Grandis, M.; Nobbio, L.; Abbruzzese, M.; Banchi, L.; Minuto, F.; Barreca, A.; Garrone, S.; Mancardi, G. L.; Schenone, A. Insulin treatment enhances expression of igf-i in sural nerves of diabetic patients. Muscle Nerve 24(5):622–629; 2001.
15. Gupta, P. K.; Chullikana, A.; Parakh, R.; Desai, S.; Das, A.; Gottipamula, S.; Krishnamurthy, S.; Anthony, N.; Pherwani, A.; Majumdar, A. S. A double blind randomized placebo controlled phase I/II study assessing the safety and efficacy of allogeneic bone marrow derived mesenchymal stem cell in critical limb ischemia. J. Transl. Med. 11:143; 2013.
16. Ii, M.; Nishimura, H.; Kusano, K. F.; Qin, G.; Yoon, Y. S.; Wecker, A.; Asahara, T.; Losordo, D. W. Neuronal nitric oxide synthase mediates statin-induced restoration of vasa nervorum and reversal of diabetic neuropathy. Circulation 112(1):93–102; 2005.
17. Iwase, T.; Nagaya, N.; Fujii, T.; Itoh, T.; Murakami, S.; Matsumoto, T.; Kangawa, K.; Kitamura, S. Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hindlimb ischemia. Cardiovasc. Res. 66(3):543–551; 2005.
18. Jackson, L.; Jones, D. R.; Scotting, P.; Sottile, V. Adult mesenchymal stem cells: Differentiation potential and therapeutic applications. J. Postgrad. Med. 53(2):121–127; 2007.
19. Jeong, J. O.; Kim, M. O.; Kim, H.; Lee, M. Y.; Kim, S. W.; Ii, M.; Lee, J. U.; Lee, J.; Choi, Y. J.; Cho, H. J. and others. Dual angiogenic and neurotrophic effects of bone marrowderived endothelial progenitor cells on diabetic neuropathy. Circulation 119(5):699–708; 2009.
20. Jessen, K. R.; Mirsky, R. Negative regulation of myelination: Relevance for development, injury, and demyelinating disease. Glia 56(14):1552–1565; 2008.
21. Kalichman, M. W.; Powell, H. C.; Mizisin, A. P. Reactive, degenerative, and proliferative Schwann cell responses in experimental galactose and human diabetic neuropathy. Acta Neuropathol. 95(1):47–56; 1998.
22. Kamihata, H.; Matsubara, H.; Nishiue, T.; Fujiyama, S.; Tsutsumi, Y.; Ozono, R.; Masaki, H.; Mori, Y.; Iba, O.; Tateishi, E., and others. Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation 104(9):1046–1052; 2001.
23. Keilhoff, G.; Stang, F.; Goihl, A.; Wolf, G.; Fansa, H. Transdifferentiated mesenchymal stem cells as alternative therapy in supporting nerve regeneration and myelination. Cell. Mol. Neurobiol. 26(7–8):1235–1252; 2006.
24. Kermani, P.; Rafii, D.; Jin, D. K.; Whitlock, P.; Schaffer, W.; Chiang, A.; Vincent, L.; Friedrich, M.; Shido, K.; Hackett, N. R. and others. Neurotrophins promote revascularization by local recruitment of trkb+ endothelial cells and systemic mobilization of hematopoietic progenitors. J. Clin. Invest. 115(3):653–663; 2005.
25. Kim, H.; Han, J. W.; Lee, J. Y.; Choi, Y. J.; Sohn, Y. D.; Song, M.; Yoon, Y. S. Diabetic mesenchymal stem cells are ineffective for improving limb ischemia due to their impaired angiogenic capability. Cell Transplant. 24(8):1571–1584; 2015.
26. Kim, H.; Park, J. S.; Choi, Y. J.; Kim, M. O.; Huh, Y. H.; Kim, S. W.; Han, J. W.; Lee, J.; Kim, S.; Houge, M. A. and others. Bone marrow mononuclear cells have neurovascular tropism and improve diabetic neuropathy. Stem Cells 27(7):1686–1696; 2009.
27. Kim, S. W.; Kim, H.; Cho, H. J.; Lee, J. U.; Levit, R.; Yoon, Y. S. Human peripheral blood-derived cd31+ cells have robust angiogenic and vasculogenic properties and are effective for treating ischemic vascular disease. J. Am. Coll. Cardiol. 56(7):593–607; 2010.
28. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Shou, M.; Lee, C. W.; Barr, S.; Fuchs, S.; Epstein, S. E. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109(12):1543–1549; 2004.
29. Kusano, K. F.; Allendoerfer, K. L.; Munger, W.; Pola, R.; Bosch-Marce, M.; Kirchmair, R.; Yoon, Y. S.; Curry, C.; Silver, M.; Kearney, M. and others. Sonic hedgehog induces arteriogenesis in diabetic vasa nervorum and restores function in diabetic neuropathy. Arterioscler. Thromb. Vasc. Biol. 24(11):2102–2107; 2004.
30. Lazarovici, P.; Marcinkiewicz, C.; Lelkes, P. I. Cross talk between the cardiovascular and nervous systems: Neurotrophic effects of vascular endothelial growth factor (vegf) and angiogenic effects of nerve growth factor (ngf)-implications in drug development. Curr. Pharm. Des. 12(21):2609–2622; 2006.
31. Leinninger, G. M.; Vincent, A. M.; Feldman, E. L. The role of growth factors in diabetic peripheral neuropathy. J. Peripher. Nerv. Syst. 9(1):26–53; 2004.
32. Lenhard, T.; Schober, A.; Suter-Crazzolara, C.; Unsicker, K. Fibroblast growth factor-2 requires glial-cell-linederived neurotrophic factor for exerting its neuroprotective actions on glutamate-lesioned hippocampal neurons. Mol. Cell. Neurosci. 20(2):181–197; 2002.
33. Liu, G. S.; Shi, J. Y.; Lai, C. L.; Hong, Y. R.; Shin, S. J.; Huang, H. T.; Lam, H. C.; Wen, Z. H.; Hsu, K. S.; Chen, C. H. and others. Peripheral gene transfer of glial cell-derived neurotrophic factor ameliorates neuropathic deficits in diabetic rats. Hum. Gene Ther. 20(7):715–727; 2009.
34. Lopez-Lopez, C.; LeRoith, D.; Torres-Aleman, I. Insulinlike growth factor I is required for vessel remodeling in the adult brain. Proc. Natl. Acad. Sci. USA 101(26):9833–9838; 2004.
35. Lu, L.; Chen, X.; Zhang, C. W.; Yang, W. L.; Wu, Y. J.; Sun, L.; Bai, L. M.; Gu, X. S.; Ahmed, S.; Dawe, G. S. and others. Morphological and functional characterization of predifferentiation of myelinating glia-like cells from human bone marrow stromal cells through activation of f3/ notch signaling in mouse retina. Stem Cells 26(2):580–590; 2008.
36. Mahay, D.; Terenghi, G.; Shawcross, S. G. Growth factors in mesenchymal stem cells following glial-cell differentiation. Biotechnol. Appl. Biochem. 51(Pt 4):167–176; 2008.
37. Mahay, D.; Terenghi, G.; Shawcross, S. G. Schwann cell mediated trophic effects by differentiated mesenchymal stem cells. Exp. Cell Res. 314(14):2692–2701; 2008.
38. Mangi, A. A.; Noiseux, N.; Kong, D.; He, H.; Rezvani, M.; Ingwall, J. S.; Dzau, V. J. Mesenchymal stem cells modified with akt prevent remodeling and restore performance of infarcted hearts. Nat. Med. 9(9):1195–1201; 2003.
39. Michailov, G. V.; Sereda, M. W.; Brinkmann, B. G.; Fischer, T. M.; Haug, B.; Birchmeier, C.; Role, L.; Lai, C.; Schwab, M. H.; Nave, K. A. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304(5671):700–703; 2004.
40. Mizisin, A. P.; Shelton, G. D.; Wagner, S.; Rusbridge, C.; Powell, H. C. Myelin splitting, Schwann cell injury and demyelination in feline diabetic neuropathy. Acta Neuropathol. 95(2):171–174; 1998.
41. Mizisin, A. P.; Vu, Y.; Shuff, M.; Calcutt, N. A. Ciliary neurotrophic factor improves nerve conduction and ameliorates regeneration deficits in diabetic rats. Diabetes 53(7):1807–1812; 2004.
42. Muller-Ehmsen, J.; Krausgrill, B.; Burst, V.; Schenk, K.; Neisen, U. C.; Fries, J. W.; Fleischmann, B. K.; Hescheler, J.; Schwinger, R. H. Effective engraftment but poor midterm persistence of mononuclear and mesenchymal bone marrow cells in acute and chronic rat myocardial infarction. J. Mol. Cell. Cardiol. 41(5):876–884; 2006.
43. Prockop, D. J. “Stemness” does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin. Pharmacol. Ther. 82(3):241–243; 2007.
44. Ravasi, M.; Scuteri, A.; Pasini, S.; Bossi, M.; Menendez, V. R.; Maggioni, D.; Tredici, G. Undifferentiated MSCs are able to myelinate drg neuron processes through p75. Exp. Cell Res. 319(19):2989–2999; 2013.
45. Said, G. Diabetic neuropathy–A review. Nat. Clin. Pract. Neurol. 3(6):331–340; 2007.
46. Salis, M. B.; Graiani, G.; Desortes, E.; Caldwell, R. B.; Madeddu, P.; Emanueli, C. Nerve growth factor supplementation reverses the impairment, induced by type 1 diabetes, of hindlimb post-ischaemic recovery in mice. Diabetologia 47(6):1055–1063; 2004.
47. Schratzberger, P.; Walter, D. H.; Rittig, K.; Bahlmann, F. H.; Pola, R.; Curry, C.; Silver, M.; Krainin, J. G.; Weinberg, D. H.; Ropper, A. H. and others. Reversal of experimental diabetic neuropathy by vegf gene transfer. J. Clin. Invest. 107(9):1083–1092; 2001.
48. Sharma, A. K.; Thomas, P. K. Peripheral nerve structure and function in experimental diabetes. J. Neurol. Sci. 23(1):1–15; 1974.
49. Shi, X.; Chen, Y.; Nadeem, L.; Xu, G. Beneficial effect of tnf-alpha inhibition on diabetic peripheral neuropathy. J. Neuroinflammation 10:69; 2013.
50. Shibata, T.; Naruse, K.; Kamiya, H.; Kozakae, M.; Kondo, M.; Yasuda, Y.; Nakamura, N.; Ota, K.; Tosaki, T.; Matsuki, T. and others. Transplantation of bone marrow-derived mesenchymal stem cells improves diabetic polyneuropathy in rats. Diabetes 57(11):3099–3107; 2008.
51. Shy, M. E. Biology of peripheral inherited neuropathies: Schwann cell axonal interactions. Adv. Exp. Med. Biol. 652:171–181; 2009.
52. Simovic, D.; Isner, J. M.; Ropper, A. H.; Pieczek, A.; Weinberg, D. H. Improvement in chronic ischemic neuropathy after intramuscular phvegf165 gene transfer in patients with critical limb ischemia. Arch. Neurol. 58(5):761–768; 2001.
53. Wellmer, A.; Misra, V. P.; Sharief, M. K.; Kopelman, P. G.; Anand, P. A double-blind placebo-controlled clinical trial of recombinant human brain-derived neurotrophic factor (rhbdnf) in diabetic polyneuropathy. J. Peripher. Nerv. Syst. 6(4):204–210; 2001.
54. Wen, Y.; Meng, L.; Xie, J.; Ouyang, J. Direct autologous bone marrow-derived stem cell transplantation for ischemic heart disease: A meta-analysis. Expert Opin. Biol. Ther. 11(5):559–567; 2011.
55. Williams, A. R.; Hare, J. M. Mesenchymal stem cells: Biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ. Res. 109(8):923–940; 2011.
56. Zacchigna, S.; Lambrechts, D.; Carmeliet, P. Neurovascular signalling defects in neurodegeneration. Nat. Rev. Neurosci. 9(3):169–181; 2008.
57. Zhang, C.; Sun, A.; Zhang, S.; Yao, K.; Wu, C.; Fu, M.; Wang, K.; Zou, Y.; Ge, J. Efficacy and safety of intracoronary autologous bone marrow-derived cell transplantation in patients with acute myocardial infarction: Insights from randomized controlled trials with 12 or more months follow- up. Clin. Cardiol. 33(6):353–360; 2010.