Intravenous administration of xenogenic adipose-derived mesenchymal stem cells (ADMSC) and ADMSC-derived exosomes markedly reduced brain infarct volume and preserved neurological function in rat after acute ischemic stroke

Oncotarget

Volumn 7, Issue 46, 2016, Pages 74537-74556

  Chen, Kuan Hung ^a,d   Chen, Chih Hung ^a   Wallace, Christopher Glenn ^b   Yuen, Chun Man ^a   Kao, Gour Shenq ^a   Chen, Yi Ling ^a   Shao, Pei Lin ^c   Chen, Yung Lung ^a   Chai, Han Tan ^a   Lin, Kun Chen ^a   Liu, Chu Feng ^a   Chang, Hsueh Wen ^d   Lee, Mel S ^a   Yip, Hon Kan ^a,c,e  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

^c ASIA UNIVERSITY   (Taiwan)

^d NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^e CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Brain infarct size; Exosomes; Ischemic stroke; Neurological function; Pathology Section; Xenogenic adipose derived mesenchymal stem cell

Indexed keywords

AQUAPORIN 4; CASPASE 3; CD11 ANTIGEN; CD68 ANTIGEN; GELATINASE B; HISTONE H2AX; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; RANTES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMAD3 PROTEIN; THY 1 ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; XRCC1 PROTEIN;

ADIPOSE DERIVED MESENCHYMAL STEM CELL DERIVED EXOSOME TRANSPLANTATION; ADIPOSE DERIVED MESENCHYMAL STEM CELL TRANSPLANTATION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL DAMAGE; CONTROLLED STUDY; CONVALESCENCE; DNA DAMAGE; HISTOPATHOLOGY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOCHONDRIAL DAMAGE; NERVOUS SYSTEM FUNCTION; NEUROANATOMY; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; SENSORIMOTOR FUNCTION; ADIPOSE TISSUE; ANIMAL; BRAIN; CEREBROVASCULAR ACCIDENT; CYTOLOGY; DISEASE MODEL; EXOSOME; INTRAVENOUS DRUG ADMINISTRATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PROCEDURES; TREATMENT OUTCOME; XENOGRAFT;

ADIPOSE TISSUE; ADMINISTRATION, INTRAVENOUS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; EXOSOMES; HETEROGRAFTS; MAGNETIC RESONANCE IMAGING; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; OXIDATIVE STRESS; RATS; STROKE; TREATMENT OUTCOME;

EID: 84996605938     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12902     Document Type: Article

References (41)

1. Holloway RG, Benesch CG, Burgin WS and Zentner JB. Prognosis and decision making in severe stroke. JAMA. 2005; 294:725-733.
2. Kelly AG, Hoskins KD and Holloway RG. Early stroke mortality, patient preferences, and the withdrawal of care bias. Neurology. 2012; 79:941-944.
3. Kharitonova T, Ahmed N, Thoren M, Wardlaw JM, von Kummer R, Glahn J and Wahlgren N. Hyperdense middle cerebral artery sign on admission CT scan-prognostic significance for ischaemic stroke patients treated with intravenous thrombolysis in the safe implementation of thrombolysis in Stroke International Stroke Thrombolysis Register. Cerebrovasc Dis. 2009; 27:51-59.
4. Murphy SL, Xu J and Kochanek KD. Deaths: final data for 2010. Natl Vital Stat Rep. 2013; 61:1-117.
5. Adams HP, Jr., Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL and Marsh EE, 3rd. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993; 24:35-41.
6. Chen ZM, Sandercock P, Pan HC, Counsell C, Collins R, Liu LS, Xie JX, Warlow C and Peto R. Indications for early aspirin use in acute ischemic stroke: A combined analysis of 40 000 randomized patients from the chinese acute stroke trial and the international stroke trial. On behalf of the CAST and IST collaborative groups. Stroke. 2000; 31:1240-1249.
7. Grau AJ, Weimar C, Buggle F, Heinrich A, Goertler M, Neumaier S, Glahn J, Brandt T, Hacke W and Diener HC. Risk factors, outcome, and treatment in subtypes of ischemic stroke: the German stroke data bank. Stroke. 2001; 32:2559-2566.
8. Siemonsen S, Lobel U, Sedlacik J, Forkert ND, Mouridsen K, Ostergaard L, Thomalla G and Fiehler J. Elevated T2-values in MRI of stroke patients shortly after symptom onset do not predict irreversible tissue infarction. Brain. 2012; 135:1981-1989.
9. Asadi H, Dowling R, Yan B, Wong S and Mitchell P. Advances in endovascular treatment of acute ischaemic stroke. Intern Med J. 2015; 45:798-805.
10. Chen CJ, Ding D, Starke RM, Mehndiratta P, Crowley RW, Liu KC, Southerland AM and Worrall BB. Endovascular vs medical management of acute ischemic stroke. Neurology. 2015; 85:1980-1990.
11. Asadi H, Williams D and Thornton J. Changing Management of Acute Ischaemic Stroke: the New Treatments and Emerging Role of Endovascular Therapy. Curr Treat Options Neurol. 2016; 18:20.
12. Adams HP, Jr., del Zoppo G, Alberts MJ, Bhatt DL, Brass L, Furlan A, Grubb RL, Higashida RT, Jauch EC, Kidwell C, Lyden PD, Morgenstern LB, Qureshi AI, Rosenwasser RH, Scott PA, Wijdicks EF, American Heart A, American Stroke Association Stroke C, Clinical Cardiology C, Cardiovascular R, Intervention C, Atherosclerotic Peripheral Vascular D and Quality of Care Outcomes in Research Interdisciplinary Working G. Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups: the American Academy of Neurology affirms the value of this guideline as an educational tool for neurologists. Stroke. 2007; 38:1655-1711.
13. Pan Y, Wang A, Liu G, Zhao X, Meng X, Zhao K, Liu L, Wang C, Johnston SC, Wang Y, Wang Y and Investigators C. Cost-effectiveness of clopidogrel-aspirin versus aspirin alone for acute transient ischemic attack and minor stroke. J Am Heart Assoc. 2014; 3:e000912.
14. Stecksen A, Asplund K, Appelros P, Glader EL, Norrving B, Eriksson M and Riks-Stroke C. Thrombolytic therapy rates and stroke severity: an analysis of data from the Swedish stroke register (Riks-Stroke) 2007-2010. Stroke. 2012; 43:536-538.
15. Wahlgren N, Ahmed N, Davalos A, Ford GA, Grond M, Hacke W, Hennerici MG, Kaste M, Kuelkens S, Larrue V, Lees KR, Roine RO, Soinne L, Toni D, Vanhooren G and investigators S-M. Thrombolysis with alteplase for acute ischaemic stroke in the Safe Implementation of Thrombolysis in Stroke-Monitoring Study (SITS-MOST): an observational study. Lancet. 2007; 369:275-282.
16. Yeo LL, Paliwal P, Teoh HL, Seet RC, Chan BP, Liang S, Venketasubramanian N, Rathakrishnan R, Ahmad A, Ng KW, Loh PK, Ong JJ, Wakerley BR, Chong VF, Bathla G and Sharma VK. Timing of recanalization after intravenous thrombolysis and functional outcomes after acute ischemic stroke. JAMA Neurol. 2013; 70:353-358.
17. Rangel-Castilla L, Snyder KV, Siddiqui AH, Levy EI and Hopkins NL. Endovascular intracranial treatment of acute ischemic strokes. J Cardiovasc Surg (Torino). 2016; 57:36-47.
18. Minnerup J, Wersching H, Teuber A, Wellmann J, Eyding J, Weber R, Reimann G, Weber W, Krause LU, Kurth T, Berger K and Investigators R. Outcome After Thrombectomy and Intravenous Thrombolysis in Patients With Acute Ischemic Stroke: A Prospective Observational Study. Stroke. 2016; 47:1584-1592.
19. Leu S, Sun CK, Sheu JJ, Chang LT, Yuen CM, Yen CH, Chiang CH, Ko SF, Pei SN, Chua S, Youssef AA, Wu CJ and Yip HK. Autologous bone marrow cell implantation attenuates left ventricular remodeling and improves heart function in porcine myocardial infarction: an echocardiographic, six-month angiographic, and molecular-cellular study. Int J Cardiol. 2011; 150:156-168.
20. Tang XL, Rokosh G, Sanganalmath SK, Yuan F, Sato H, Mu J, Dai S, Li C, Chen N, Peng Y, Dawn B, Hunt G, Leri A, Kajstura J, Tiwari S, Shirk G, Anversa P and Bolli R. Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation. 2010; 121:293-305.
21. Chen YT, Chiang HJ, Chen CH, Sung PH, Lee FY, Tsai TH, Chang CL, Chen HH, Sun CK, Leu S, Chang HW, Yang CC and Yip HK. Melatonin treatment further improves adipose-derived mesenchymal stem cell therapy for acute interstitial cystitis in rat. J Pineal Res. 2014; 57:248-261.
22. Chen HH, Lin KC, Wallace CG, Chen YT, Yang CC, Leu S, Chen YC, Sun CK, Tsai TH, Chen YL, Chung SY, Chang CL and Yip HK. Additional benefit of combined therapy with melatonin and apoptotic adipose-derived mesenchymal stem cell against sepsis-induced kidney injury. J Pineal Res. 2014; 57:16-32.
23. Yip HK, Chang YC, Wallace CG, Chang LT, Tsai TH, Chen YL, Chang HW, Leu S, Zhen YY, Tsai CY, Yeh KH, Sun CK and Yen CH. Melatonin treatment improves adipose-derived mesenchymal stem cell therapy for acute lung ischemia-reperfusion injury. J Pineal Res. 2013; 54:207-221.
24. Chen HH, Chang CL, Lin KC, Sung PH, Chai HT, Zhen YY, Chen YC, Wu YC, Leu S, Tsai TH, Chen CH, Chang HW and Yip HK. Melatonin augments apoptotic adipose-derived mesenchymal stem cell treatment against sepsis-induced acute lung injury. Am J Transl Res. 2014; 6:439-458.
25. Lin KC, Yip HK, Shao PL, Wu SC, Chen KH, Chen YT, Yang CC, Sun CK, Kao GS, Chen SY, Chai HT, Chang CL, Chen CH and Lee MS. Combination of adipose-derived mesenchymal stem cells (ADMSC) and ADMSC-derived exosomes for protecting kidney from acute ischemia-reperfusion injury. Int J Cardiol. 2016; 216:173-185.
26. Chen HH, Lai PF, Lan YF, Cheng CF, Zhong WB, Lin YF, Chen TW and Lin H. Exosomal ATF3 RNA attenuates pro-inflammatory gene MCP-1 transcription in renal ischemia-reperfusion. J Cell Physiol. 2014; 229:1202-1211.
27. Zou X, Zhang G, Cheng Z, Yin D, Du T, Ju G, Miao S, Liu G, Lu M and Zhu Y. Microvesicles derived from human Wharton's Jelly mesenchymal stromal cells ameliorate renal ischemia-reperfusion injury in rats by suppressing CX3CL1. Stem Cell Res Ther. 2014; 5:40.
28. Gatti S, Bruno S, Deregibus MC, Sordi A, Cantaluppi V, Tetta C and Camussi G. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant. 2011; 26:1474-1483.
29. Dorronsoro A and Robbins PD. Regenerating the injured kidney with human umbilical cord mesenchymal stem cell-derived exosomes. Stem Cell Res Ther. 2013; 4:39.
30. Tyack PL, Calambokidis J, Friedlaender A, Goldbogen J and Southall B. Formal Comment on Schorr GS, Falcone EA, Moretti DJ, Andrews RD (2014) First Long-Term Behavioral Records from Cuvier's Beaked Whales (Ziphius cavirostris) Reveal Record-Breaking Dives. PLoS ONE 9(3): e92633. doi:10.1371/journal.pone.0092633. PLoS One. 2015; 10:e0142287.
31. Ko SF, Yip HK, Zhen YY, Lee CC, Lee CC, Huang CC, Ng SH and Lin JW. Adipose-Derived Mesenchymal Stem Cell Exosomes Suppress Hepatocellular Carcinoma Growth in a Rat Model: Apparent Diffusion Coefficient, Natural Killer T-Cell Responses, and Histopathological Features. Stem Cells Int. 2015; 2015:853506.
32. Leu S, Lin YC, Yuen CM, Yen CH, Kao YH, Sun CK and Yip HK. Adipose-derived mesenchymal stem cells markedly attenuate brain infarct size and improve neurological function in rats. J Transl Med. 2010; 8:63.
33. Lambert JM, Lopez EF and Lindsey ML. Macrophage roles following myocardial infarction. Int J Cardiol. 2008; 130:147-158.
34. Frangogiannis NG. The immune system and cardiac repair. Pharmacol Res. 2008; 58:88-111.
35. Sheu JJ, Chua S, Sun CK, Chang LT, Yen CH, Wu CJ, Fu M and Yip HK. Intra-coronary administration of cyclosporine limits infarct size, attenuates remodeling and preserves left ventricular function in porcine acute anterior infarction. Int J Cardiol. 2011; 147:79-87.
36. Chen YL, Tsai TH, Wallace CG, Chen YL, Huang TH, Sung PH, Yuen CM, Sun CK, Lin KC, Chai HT, Sheu JJ, Lee FY and Yip HK. Intra-carotid arterial administration of autologous peripheral blood-derived endothelial progenitor cells improves acute ischemic stroke neurological outcomes in rats. Int J Cardiol. 2015; 201:668-683.
37. Yuen CM, Chung SY, Tsai TH, Sung PH, Huang TH, Chen YL, Chen YL, Chai HT, Zhen YY, Chang MW, Wang CJ, Chang HW, Sun CK and Yip HK. Extracorporeal shock wave effectively attenuates brain infarct volume and improves neurological function in rat after acute ischemic stroke. Am J Transl Res. 2015; 7:976-994.
38. Chen HH, Chen YT, Yang CC, Chen KH, Sung PH, Chiang HJ, Chen CH, Chua S, Chung SY, Chen YL, Huang TH, Kao GS, Chen SY, Lee MS and Yip HK. Melatonin pretreatment enhances the therapeutic effects of exogenous mitochondria against hepatic ischemia-reperfusion injury in rats through suppression of mitochondrial permeability transition. J Pineal Res. 2016; 61:52-68.
39. Chen YT, Yang CC, Zhen YY, Wallace CG, Yang JL, Sun CK, Tsai TH, Sheu JJ, Chua S, Chang CL, Cho CL, Leu S and Yip HK. Cyclosporine-assisted adipose-derived mesenchymal stem cell therapy to mitigate acute kidney ischemia-reperfusion injury. Stem Cell Res Ther. 2013; 4:62.
40. Fan H, Goodwin AJ, Chang E, Zingarelli B, Borg K, Guan S, Halushka PV and Cook JA. Endothelial progenitor cells and a stromal cell-derived factor-1alpha analogue synergistically improve survival in sepsis. Am J Respir Crit Care Med. 2014; 189:1509-1519.
41. Masuda H, Tanaka R, Fujimura S, Ishikawa M, Akimaru H, Shizuno T, Sato A, Okada Y, Iida Y, Itoh J, Itoh Y, Kamiguchi H, Kawamoto A and Asahara T. Vasculogenic conditioning of peripheral blood mononuclear cells promotes endothelial progenitor cell expansion and phenotype transition of anti-inflammatory macrophage and T lymphocyte to cells with regenerative potential. J Am Heart Assoc. 2014; 3:e000743.