Therapeutic benefits of intravenous cardiosphere-derived cell therapy in rats with pulmonary hypertension

PLoS ONE

Volumn 12, Issue 8, 2017, Pages

  Middleton, Ryan C ^a   Fournier, Mario ^a   Xu, Xuan ^a   Marbán, Eduardo ^a   Lewis, Michael I ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCROTALINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTERIAL GAS; ARTERIAL WALL THICKNESS; ARTERIOLE; ARTICLE; BODY WEIGHT; CARDIAC STEM CELL; CARDIOSPHERE DERIVED CELL THERAPY; CELL INFILTRATION; CELL PROLIFERATION; CELL THERAPY; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENDOTHELIAL DYSFUNCTION; HEART HEMODYNAMICS; HEART OUTPUT; HEART RIGHT VENTRICLE; HEART RIGHT VENTRICLE HYPERTROPHY; HEART RIGHT VENTRICLE PRESSURE; HEART VENTRICLE REMODELING; IMMUNOHISTOCHEMISTRY; IMMUNOHISTOLOGY; IMMUNOMODULATION; LUNG ALVEOLUS MACROPHAGE; LYMPHOCYTIC INFILTRATION; MALE; NONHUMAN; PULMONARY HYPERTENSION; RAT; ANIMAL; BIOLOGICAL THERAPY; DIAGNOSTIC IMAGING; HYPERTENSION, PULMONARY; SPRAGUE DAWLEY RAT;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; ECHOCARDIOGRAPHY; HYPERTENSION, PULMONARY; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85028411307     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0183557     Document Type: Article

References (37)

1. Rabinovitch M. Molecular pathogenesis of pulmonary arterial hypertension. J Clin Invest. 2012 Dec; 122(12):4306–13. https://doi.org/10.1172/JCI60658 PMID: 23202738
2. Rabinovitch M, Guignabert C, Humbert M, Nicolls MR. Inflammation and immunity in the pathogenesis of pulmonary arterial hypertension. Circ Res. 2014 Jun 20; 115(1):165–75. https://doi.org/10.1161/CIRCRESAHA.113.301141 PMID: 24951765
3. van de Veerdonk MC, Kind T, Marcus JT, Mauritz G-J, Heymans MW, Bogaard H-J, et al. Progressive right ventricular dysfunction in patients with pulmonary arterial hypertension responding to therapy. J Am Coll Cardiol. 2011 Dec 6; 58(24):2511–9. https://doi.org/10.1016/j.jacc.2011.06.068 PMID: 22133851
4. Humbert M, Sitbon O, Yaïci A, Montani D, O’Callaghan DS, Jaïs X, et al. Survival in incident and prevalent cohorts of patients with pulmonary arterial hypertension. Eur Respir J. 2010 Sep; 36(3):549–55. https://doi.org/10.1183/09031936.00057010 PMID: 20562126
5. Farber HW, Miller DP, Poms AD, Badesch DB, Frost AE, Muros-Le Rouzic E, et al. Five-Year outcomes of patients enrolled in the REVEAL Registry. Chest. 2015 Oct; 148(4):1043–54. https://doi.org/10.1378/chest.15-0300 PMID: 26066077
6. Barst RJ, Chung L, Zamanian RT, Turner M, McGoon MD. Functional class improvement and 3-year survival outcomes in patients with pulmonary arterial hypertension in the REVEAL Registry. Chest. 2013 Jul; 144(1):160–8. https://doi.org/10.1378/chest.12-2417 PMID: 23429998
7. Stacher E, Graham BB, Hunt JM, Gandjeva A, Groshong SD, McLaughlin VV, et al. Modern age pathology of pulmonary arterial hypertension. Am J Respir Crit Care Med. 2012 Aug 1; 186(3):261–72. https://doi.org/10.1164/rccm.201201-0164OC PMID: 22679007
8. Suen CM, Mei SHJ, Kugathasan L, Stewart DJ. Targeted delivery of genes to endothelial cells and cell- and gene-based therapy in pulmonary vascular diseases. Compr Physiol. 2013 Oct; 3(4):1749–79. https://doi.org/10.1002/cphy.c120034 PMID: 24265244
9. Malliaras K, Li T-S, Luthringer D, Terrovitis J, Cheng K, Chakravarty T, et al. Safety and Efficacy of Allo-geneic Cell Therapy in Infarcted Rats Transplanted with Mismatched Cardiosphere-Derived Cells. Circulation. 2012 Jan 3; 125(1):100–12. https://doi.org/10.1161/CIRCULATIONAHA.111.042598 PMID: 22086878
10. Aminzadeh MA, Tseliou E, Sun B, Cheng K, Malliaras K, Makkar RR, et al. Therapeutic efficacy of car-diosphere-derived cells in a transgenic mouse model of non-ischaemic dilated cardiomyopathy. Eur Heart J. 2015 Mar 21; 36(12):751–62. https://doi.org/10.1093/eurheartj/ehu196 PMID: 24866210
11. de Couto G, Liu W, Tseliou E, Sun B, Makkar N, Kanazawa H, et al. Macrophages mediate cardiopro-tective cellular postconditioning in acute myocardial infarction. J Clin Invest. 2015 Aug 3; 125(8):3147–62. https://doi.org/10.1172/JCI81321 PMID: 26214527
12. Gallet R, de Couto G, Simsolo E, Valle J, Sun B, Liu W, et al. Cardiosphere-derived cells reverse heart failure with preserved ejection fraction (HFpEF) in rats by decreasing fibrosis and inflammation. JACC Basic Transl Sci. 2016 Feb; 1(1–2):14–28. https://doi.org/10.1016/j.jacbts.2016.01.003 PMID: 27104217
13. Tseliou E, Fouad J, Reich H, Slipczuk L, de Couto G, Aminzadeh M, et al. Fibroblasts Rendered Antifi-brotic, Antiapoptotic, and Angiogenic by Priming With Cardiosphere-Derived Extracellular Membrane Vesicles. J Am Coll Cardiol. 2015 Aug 11; 66(6):599–611. https://doi.org/10.1016/j.jacc.2015.05.068PMID: 26248985
14. Ibrahim AG-E, Cheng K, Marbán E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Rep. 2014 May 6; 2(5):606–19.
15. Davis DR, Kizana E, Terrovitis J, Barth AS, Zhang Y, Smith RR, et al. Isolation and expansion of functionally-competent cardiac progenitor cells directly from heart biopsies. J Mol Cell Cardiol. 2010 Aug; 49 (2):312–21. https://doi.org/10.1016/j.yjmcc.2010.02.019 PMID: 20211627
16. Tian W, Jiang X, Tamosiuniene R, Sung YK, Qian J, Dhillon G, et al. Blocking macrophage leukotriene b4 prevents endothelial injury and reverses pulmonary hypertension. Sci Transl Med. 2013 Aug 28; 5 (200):200ra117. https://doi.org/10.1126/scitranslmed.3006674 PMID: 23986401
17. Voelkel NF, Tamosiuniene R, Nicolls MR. Challenges and opportunities in treating inflammation associated with pulmonary hypertension. Expert Rev Cardiovasc Ther. 2016 Aug; 14(8):939–51. https://doi.org/10.1080/14779072.2016.1180976 PMID: 27096622
18. Schermuly RT, Kreisselmeier KP, Ghofrani HA, Yilmaz H, Butrous G, Ermert L, et al. Chronic sildenafil treatment inhibits monocrotaline-induced pulmonary hypertension in rats. Am J Respir Crit Care Med. 2004 Jan 1; 169(1):39–45. https://doi.org/10.1164/rccm.200302-282OC PMID: 12958054
19. Perros F, Dorfmüller P, Souza R, Durand-Gasselin I, Mussot S, Mazmanian M, et al. Dendritic cell recruitment in lesions of human and experimental pulmonary hypertension. Eur Respir J. 2007 Mar; 29 (3):462–8. https://doi.org/10.1183/09031936.00094706 PMID: 17107989
20. Stenmark KR, Meyrick B, Galie N, Mooi WJ, McMurtry IF. Animal models of pulmonary arterial hypertension: the hope for etiological discovery and pharmacological cure. Am J Physiol Lung Cell Mol Physiol. 2009 Dec; 297(6):L1013–1032. https://doi.org/10.1152/ajplung.00217.2009 PMID: 19748998
21. Perros F, Dorfmüller P, Souza R, Durand-Gasselin I, Godot V, Capel F, et al. Fractalkine-induced smooth muscle cell proliferation in pulmonary hypertension. Eur Respir J. 2007 May; 29(5):937–43. https://doi.org/10.1183/09031936.00104706 PMID: 17182651
22. Le Hiress M, Tu L, Ricard N, Phan C, Thuillet R, Fadel E, et al. Proinflammatory Signature of the Dysfunctional Endothelium in Pulmonary Hypertension. Role of the Macrophage Migration Inhibitory Factor/CD74 Complex. Am J Respir Crit Care Med. 2015 Oct 15; 192(8):983–97. https://doi.org/10.1164/rccm.201402-0322OC PMID: 26203495
23. Huang W-C, Ke M-W, Cheng C-C, Chiou S-H, Wann S-R, Shu C-W, et al. Therapeutic Benefits of Induced Pluripotent Stem Cells in Monocrotaline-Induced Pulmonary Arterial Hypertension. PloS One. 2016; 11(2):e0142476. https://doi.org/10.1371/journal.pone.0142476 PMID: 26840075
24. Price LC, Montani D, Tcherakian C, Dorfmüller P, Souza R, Gambaryan N, et al. Dexamethasone reverses monocrotaline-induced pulmonary arterial hypertension in rats. Eur Respir J. 2011 Apr; 37 (4):813–22. https://doi.org/10.1183/09031936.00028310 PMID: 20693255
25. Reindel JF, Ganey PE, Wagner JG, Slocombe RF, Roth RA. Development of morphologic, hemodynamic, and biochemical changes in lungs of rats given monocrotaline pyrrole. Toxicol Appl Pharmacol. 1990 Nov; 106(2):179–200. PMID: 2256110
26. Huang J, Wolk JH, Gewitz MH, Mathew R. Progressive endothelial cell damage in an inflammatory model of pulmonary hypertension. Exp Lung Res. 2010 Feb; 36(1):57–66. https://doi.org/10.3109/ 01902140903104793 PMID: 20128682
27. Long L, Crosby A, Yang X, Southwood M, Upton PD, Kim D-K, et al. Altered bone morphogenetic protein and transforming growth factor-beta signaling in rat models of pulmonary hypertension: potential for activin receptor-like kinase-5 inhibition in prevention and progression of disease. Circulation. 2009 Feb 3; 119(4):566–76. https://doi.org/10.1161/CIRCULATIONAHA.108.821504 PMID: 19153267
28. Zhao YD, Courtman DW, Deng Y, Kugathasan L, Zhang Q, Stewart DJ. Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells: efficacy of combined cell and eNOS gene therapy in established disease. Circ Res. 2005 Mar 4; 96 (4):442–50. https://doi.org/10.1161/01.RES.0000157672.70560.7b PMID: 15692087
29. Chimenti I, Smith RR, Li T-S, Gerstenblith G, Messina E, Giacomello A, et al. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res. 2010 Mar 19; 106(5):971–80. https://doi.org/10.1161/CIRCRESAHA.109.210682PMID: 20110532
30. Malliaras K, Smith RR, Kanazawa H, Yee K, Seinfeld J, Tseliou E, et al. Validation of contrast-enhanced magnetic resonance imaging to monitor regenerative efficacy after cell therapy in a porcine model of convalescent myocardial infarction. Circulation. 2013 Dec 24; 128(25):2764–75. https://doi.org/10.1161/CIRCULATIONAHA.113.002863 PMID: 24061088
31. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, et al. Regenerative potential of cardio-sphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation. 2007 Feb 20; 115(7):896–908. https://doi.org/10.1161/CIRCULATIONAHA.106.655209 PMID: 17283259
32. Blázquez R, Sánchez-Margallo FM, Crisóstomo V, Báez C, Maestre J, Álvarez V, et al. Intrapericardial Delivery of Cardiosphere-Derived Cells: An Immunological Study in a Clinically Relevant Large Animal Model. PloS One. 2016; 11(2):e0149001. https://doi.org/10.1371/journal.pone.0149001 PMID: 26866919
33. Li T-S, Cheng K, Malliaras K, Smith RR, Zhang Y, Sun B, et al. Direct comparison of different stem cell types and subpopulations reveals superior paracrine potency and myocardial repair efficacy with cardio-sphere-derived cells. J Am Coll Cardiol. 2012 Mar 6; 59(10):942–53. https://doi.org/10.1016/j.jacc.2011.11.029 PMID: 22381431
34. Meyrick B, Gamble W, Reid L. Development of Crotalaria pulmonary hypertension: hemodynamic and structural study. Am J Physiol. 1980 Nov; 239(5):H692–702. PMID: 6449154
35. Baber SR, Deng W, Master RG, Bunnell BA, Taylor BK, Murthy SN, et al. Intratracheal mesenchymal stem cell administration attenuates monocrotaline-induced pulmonary hypertension and endothelial dysfunction. Am J Physiol Heart Circ Physiol. 2007 Feb; 292(2):H1120–1128. https://doi.org/10.1152/ajpheart.00173.2006 PMID: 16980338
36. Takemiya K, Kai H, Yasukawa H, Tahara N, Kato S, Imaizumi T. Mesenchymal stem cell-based prostacyclin synthase gene therapy for pulmonary hypertension rats. Basic Res Cardiol. 2010 May; 105 (3):409–17. https://doi.org/10.1007/s00395-009-0065-8 PMID: 19838762
37. Zhou L, Chen Z, Vanderslice P, So S-P, Ruan K-H, Willerson JT, et al. Endothelial-like progenitor cells engineered to produce prostacyclin rescue monocrotaline-induced pulmonary arterial hypertension and provide right ventricle benefits. Circulation. 2013 Aug 27; 128(9):982–94. https://doi.org/10.1161/CIRCULATIONAHA.113.003139 PMID: 23841984