Therapeutic potential of adipose stem cell-derived conditioned medium against pulmonary hypertension and lung fibrosis

British Journal of Pharmacology

Volumn , Issue , 2016, Pages 2859-2879

  Rathinasabapathy, Anandharajan ^a,c   Bruce, Erin ^a   Espejo, Andrew ^a   Horowitz, Alana ^a   Sudhan, Dhivya R ^a   Nair, Anand ^b,d   Guzzo, Dominic ^a   Francis, Joseph ^b   Raizada, Mohan K ^a   Shenoy, Vinayak ^a,e   Katovich, Michael J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF IOWA   (United States)

^e California Health Sciences University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE DERIVED STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOPULMONARY HEMODYNAMICS; CELLULAR DISTRIBUTION; CONDITIONED MEDIUM; CONTROLLED STUDY; ECHOCARDIOGRAPHY; GENE EXPRESSION REGULATION; HEART; HEART MUSCLE FIBROSIS; HEART RIGHT VENTRICLE HYPERTROPHY; HEART RIGHT VENTRICULAR FIBROSIS; HISTOPATHOLOGY; INFLAMMATION; LUNG BLOOD FLOW; LUNG FIBROSIS; LUNG PARENCHYMA; MALE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PULMONARY HYPERTENSION; PULMONARY VESSEL WALL THICKNESS; RAT; RESPIRATORY TRACT PARAMETERS; RNA ANALYSIS; STEM CELL TRANSPLANTATION; UPREGULATION;

EID: 84987763886     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13562     Document Type: Article

References (66)

1. Akhavein F, St-Michel EJ, Seifert E, Rohlicek CV (2007). Decreased left ventricular function, myocarditis, and coronary arteriolar medial thickening following monocrotaline administration in adult rats. J Appl Physiol (1985) 103: 287–295.
2. Alexander SPH, Kelly E, Marrion N, Peters JA, Benson HE, Faccenda E et al. (2015a). The Concise Guide to PHARMACOLOGY 2015/16: Overview. Br J Pharmacol 172: 5729–5143.
3. Alexander SPH, Davenport AP, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015b). The Concise Guide to PHARMACOLOGY 2015/16: G protein-coupled receptors. Br J Pharmacol 172: 5744–5869.
4. Alexander SPH, Fabbro D, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015c). The Concise Guide to PHARMACOLOGY 2015/16: Catalytic receptors. Br J Pharmacol 172: 5979–6023.
5. Alexander SPH, Fabbro D, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015d). The Concise Guide to PHARMACOLOGY 2015/16: Enzymes. Br J Pharmacol 172: 6024–6109.
6. Anversa P, Perrella MA, Kourembanas S, Choi AM, Loscalzo J (2012). Regenerative pulmonary medicine: potential and promise, pitfalls and challenges. Eur J Clin Invest 42: 900–913.
7. Ashcroft T, Simpson JM, Timbrell V (1988). Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 41: 467–470.
8. Bauer EM, Shapiro R, Zheng H, Ahmad F, Ishizawar D, Comhair SA et al. (2012). High mobility group box 1 contributes to the pathogenesis of experimental pulmonary hypertension via activation of Toll-like receptor 4. Mol Med 18: 1509–1518.
9. Blaber SP, Webster RA, Hill CJ, Breen EJ, Kuah D, Vesey G et al. (2012). Analysis of in vitro secretion profiles from adipose-derived cell populations. J Transl Med 10: 172.
10. Blazquez R, Sanchez-Margallo FM, de la Rosa O, Dalemans W, Alvarez V, Tarazona R et al. (2014). Immunomodulatory potential of human adipose mesenchymal stem cells derived exosomes on in vitro stimulated T Cells. Front Immunol 5: 556. doi:10.3389/fimmu.2014.00556.
11. Brunner F, Wolkart G, Haleen S (2002). Defective intracellular calcium handling in monocrotaline-induced right ventricular hypertrophy: protective effect of long-term endothelin-A receptor blockade with 2-benzo[1,3]dioxol-5-yl-3-benzyl-4-(4-methoxy-phenyl-)- 4-oxobut-2-enoate-sodium (PD 155080). J Pharmacol Exp Ther 300: 442–449.
12. Curtis MJ, Bond RA, Spina D, Ahluwalia A, Alexander SP, Giembycz MA et al. (2015). Experimental design and analysis and their reporting: new guidance for publication in BJP. Br J Pharmacol 172: 3461–3471.
13. D'Alessio FR, Zhong Q, Jenkins J, Moldobaeva A, Wagner EM (2015). Lung angiogenesis requires CD4(+)Forkhead homeobox protein-3(+) regulatory T cells. Am J Respir Cell Mol Biol 52: 603–610.
14. Dabestani A, Mahan G, Gardin JM, Takenaka K, Burn C, Allfie A et al. (1987). Evaluation of pulmonary artery pressure and resistance by pulsed Doppler echocardiography. Am J Cardiol 59: 662–668.
15. Dardalhon V, Awasthi A, Kwon H, Galileos G, Gao W, Sobel RA et al. (2008). IL-4 inhibits TGF-beta-induced Foxp3+ T cells and, together with TGF-beta, generates IL-9+ IL-10+ Foxp3(−) effector T cells. Nat Immunol 9: 1347–1355.
16. Eguchi M, Ikeda S, Kusumoto S, Sato D, Koide Y, Kawano H et al. (2014). Adipose-derived regenerative cell therapy inhibits the progression of monocrotaline-induced pulmonary hypertension in rats. Life Sci 118: 306–312.
17. Fernandez IE, Eickelberg O (2012). New cellular and molecular mechanisms of lung injury and fibrosis in idiopathic pulmonary fibrosis. Lancet 380: 680–688.
18. Furuya N, Takenaga M, Ohta Y, Tokura Y, Hamaguchi A, Sakamaki A et al. (2012). Cell therapy with adipose tissue-derived stem/stromal cells for elastase-induced pulmonary emphysema in rats. Regen Med 7: 503–512.
19. Gonzalez-Rey E, Gonzalez MA, Varela N, O'Valle F, Hernandez-Cortes P, Rico L et al. (2010). Human adipose-derived mesenchymal stem cells reduce inflammatory and T cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann Rheum Dis 69: 241–248.
20. Habiel DM, Hogaboam C (2014). Heterogeneity in fibroblast proliferation and survival in idiopathic pulmonary fibrosis. Front Pharmacol 5: 1–6.
21. Hameed AG, Arnold ND, Chamberlain J, Pickworth JA, Paiva C, Dawson S et al. (2012). Inhibition of tumor necrosis factor-related apoptosis-inducing cie (TRAIL) reverses experimental pulmonary hypertension. J Exp Med 209: 1919–1935.
22. Hesslinger C, Strub A, Boer R, Ulrich WR, Lehner MD, Braun C. (2012). Inhibition of inducible nitric oxide synthase in respiratory diseases. Biochem Soc Trans 37: 886–891.
23. Humbert M, Sitbon O, Yaici A, Montani D, O'Callaghan DS, Jais X et al. (2010). Survival in incident and prevalent cohorts of patients with pulmonary arterial hypertension. Eur Respir J 36: 549–555.
24. Ikegame Y, Yamashita K, Hayashi S, Mizuno H, Tawada M, You F et al. (2011). Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy. Cytotherapy 13: 675–685.
25. Jeon D, Chu K, Lee ST, Jung KH, Ban JJ, Park DK et al. (2013). Neuroprotective effect of a cell-free extract derived from human adipose stem cells in experimental stroke models. Neurobiol Dis 54: 414–420.
26. Jeon D, Chu K, Lee ST, Jung KH, Kang KM, Ban JJ et al. (2011). A cell-free extract from human adipose stem cells protects mice against epilepsy. Epilepsia 52: 1617–1626.
27. Jone PN, Hinzman J, Wagner BD, Ivy DD, Younoszai A (2014). Right ventricular to left ventricular diameter ratio at end-systole in evaluating outcomes in children with pulmonary hypertension. J Am Soc Echocardiogr 27: 172–178.
28. Jopling C, Boue S, Izpisua Belmonte JC (2011). Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration. Nat Rev Mol Cell Biol 12: 79–89.
29. Kanki-Horimoto S, Horimoto H, Mieno S, Kishida K, Watanabe F, Furuya E et al. (2006). Implantation of mesenchymal stem cells overexpressing endothelial nitric oxide synthase improves right ventricular impairments caused by pulmonary hypertension. Circulation 114: I181–I185.
30. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577–1579.
31. Kim EH, Heo CY (2014). Current applications of adipose-derived stem cells and their future perspectives. World J Stem Cells 6: 65–68.
32. Lee SH, Lee EJ, Lee SY, Kim JH, Shim JJ, Shin C et al. (2014). The effect of adipose stem cell therapy on pulmonary fibrosis induced by repetitive intratracheal bleomycin in mice. Exp Lung Res 40: 117–125.
33. Leto Barone AA, Khalifian S, Lee WP, Brandacher G (2013). Immunomodulatory effects of adipose-derived stem cells: fact or fiction? Biomed Res Int 2013: 383685. http://dx.doi.org/10.1155/2013/383685.
34. Luo L, Lin T, Zheng S, Xie Z, Chen M, Lian G et al. (2015). Adipose-derived stem cells attenuate pulmonary arterial hypertension and ameliorate pulmonary arterial remodeling in monocrotaline-induced pulmonary hypertensive rats. Clin Exp Hypertens 37: 241–248.
35. McGrath JC, Lilley E (2015). Implementing guidelines on reporting research using animals (ARRIVE etc.): new requirements for publication in BJP. Br J Pharmacol 172: 3189–3193.
36. McNulty K, Janes SM (2012). Stem cells and pulmonary fibrosis: cause or cure? Proc Am Thorac Soc 9: 164–171.
37. Meyer DM, Dustin ML, Carron CP (1995). Characterization of intercellular adhesion molecule-1 ectodomain (sICAM-1) as an inhibitor of lymphocyte function-associated molecule-1 interaction with ICAM-1. J Immunol 155: 3578–3584.
38. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K et al. (2009). Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15: 42–49.
39. Nikam VS, Schermuly RT, Dumitrascu R, Weissmann N, Kwapiszewska G, Morrell N et al. (2010). Treprostinil inhibits the recruitment of bone marrow-derived circulating fibrocytes in chronic hypoxic pulmonary hypertension. Eur Respir J 36: 1302–1314.
40. O'Callaghan DS, Savale L, Montani D, Jais X, Sitbon O, Simonneau G et al. (2011). Treatment of pulmonary arterial hypertension with targeted therapies. Nat Rev Cardiol 8: 526–538.
41. Okano H, Nakamura M, Yoshida K, Okada Y, Tsuji O, Nori S et al. (2013). Steps toward safe cell therapy using induced pluripotent stem cells. Circ Res 112: 523–533.
42. Paul A, Srivastava S, Chen G, Shum-Tim D, Prakash S (2013). Functional assessment of adipose stem cells for xenotransplantation using myocardial infarction immunocompetent models: comparison with bone marrow stem cells. Cell Biochem Biophys 67: 263–273.
43. Phillips RJ, Burdick MD, Hong K, Lutz MA, Murray LA, Xue YY et al. (2004). Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J Clin Invest 114: 438–446.
44. Price LC, Wort SJ, Perros F, Dorfmuller P, Huertas A, Montani D et al. (2012). Inflammation in pulmonary arterial hypertension. Chest 141: 210–221.
45. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK et al. (2011). An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 183: 788–824.
46. Ribeiro CA, Fraga JS, Graos M, Neves NM, Reis RL, Gimble JM et al. (2012). The secretome of stem cells isolated from the adipose tissue and Wharton jelly acts differently on central nervous system derived cell populations. Stem Cell Res Ther 3: 18. doi:10.1186/scrt109.
47. Ricard N, Tu L, Le Hiress M, Huertas A, Phan C, Thuillet R et al. (2014). Increased pericyte coverage mediated by endothelial-derived fibroblast growth factor-2 and interleukin-6 is a source of smooth muscle-like cells in pulmonary hypertension. Circulation 129: 1586–1597.
48. Sabin K, Kikyo N (2014). Microvesicles as mediators of tissue regeneration. Transl Res 163: 286–295.
49. Sakao S, Taraseviciene-Stewart L, Wood K, Cool CD, Voelkel NF (2006). Apoptosis of pulmonary microvascular endothelial cells stimulates vascular smooth muscle cell growth. Am J Physiol Lung Cell Mol Physiol 291: L362–L368.
50. Salgado AJ, Reis RL, Sousa NJ, Gimble JM (2010). Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther 5: 103–110.
51. Savai R, Pullamsetti SS, Kolbe J, Bieniek E, Voswinckel R, Fink L et al. (2012). Immune and inflammatory cell involvement in the pathology of idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 186: 897–908.
52. Schermuly RT, Ghofrani HA, Wilkins MR, Grimminger F (2011). Mechanisms of disease: pulmonary arterial hypertension. Nat Rev Cardiol 8: 443–455.
53. Serrano-Mollar A, Nacher M, Gay-Jordi G, Closa D, Xaubet A, Bulbena O (2007). Intratracheal transplantation of alveolar type II cells reverses bleomycin-induced lung fibrosis. Am J Respir Crit Care Med 176: 1261–1268.
54. Shenoy V, Ferreira AJ, Qi Y, Fraga-Silva RA, Díez-Freire C, Dooies A et al. (2010). The angiotensin-converting enzyme 2/angiogenesis-(1-7)/Mas axis confers cardiopulmonary protection against lung fibrosis and pulmonary hypertension. Am J Respir Crit Care Med 182: 1065–1072.
55. Shenoy V, Kwon KC, Rathinasabapathy A, Lin S, Jin G, Song C et al. (2014). Oral delivery of angiotensin-converting enzyme 2 and angiotensin-(1-7) bioencapsulated in plant cells attenuates pulmonary hypertension. Hypertension 64: 1248–1259.
56. Shih CH, van Eeden SF, Goto Y, Hogg JC (2005). CCL23/myeloid progenitor inhibitory factor-1 inhibits production and release of polymorphonuclear leukocytes and monocytes from the bone marrow. Exp Hematol 33: 1101–1108.
57. Somanna NK, Worner PM, Murthy SN, Pankey EA, Schachtele DJ, St Hilaire RC et al. (2014). Intratracheal administration of cyclooxygenase-1-transduced adipose tissue-derived stem cells ameliorates monocrotaline-induced pulmonary hypertension in rats. Am J Physiol Heart Circ Physiol 307: H1187–H1195.
58. Southan C, Sharman JL, Benson HE, Faccenda E, Pawson AJ, Alexander SP et al. (2016). The IUPHAR/BPS Guide to PHARMACOLOGY in 2016: towards curated quantitative interactions between 1300 protein targets and 6000 cies. Nucl Acids Res 44: D1054–D1068.
59. Takemiya K, Kai H, Yasukawa H, Tahara N, Kato S, Imaizumi T (2010). Mesenchymal stem cell-based prostacyclin synthase gene therapy for pulmonary hypertension rats. Basic Res Cardiol 105: 409–417.
60. Vieillard-Baron A, Frisdal E, Raffestin B, Baker AH, Eddahibi S, Adnot S et al. (2003). Inhibition of matrix metalloproteinases by lung TIMP-1 gene transfer limits monocrotaline-induced pulmonary vascular remodeling in rats. Hum Gene Ther 14: 861–869.
61. Voelkel NF, Gomez-Arroyo J (2014). The role of vascular endothelial growth factor in pulmonary arterial hypertension. The angiogenesis paradox. Am J Respir Cell Mol Biol 51: 474–484.
62. Weidt C, Niggemann B, Kasenda B, Drell TL, Zanker KS, Dittmar T (2007). Stem cell migration: a quintessential stepping stone to successful therapy. Curr Stem Cell Res Ther 2: 89–103.
63. Young KC, Torres E, Hatzistergos KE, Hehre D, Suguihara C, Hare JM (2009). Inhibition of the SDF-1/CXCR4 axis attenuates neonatal hypoxia-induced pulmonary hypertension. Circ Res 104: 1293–1301.
64. Zaiman AL, Podowski M, Medicherla S, Gordy K, Xu F, Zhen L et al. (2008). Role of the TGF-beta/Alk5 signaling pathway in monocrotaline-induced pulmonary hypertension. Am J Respir Crit Care Med 177: 896–905.
65. Zhao YD, Courtman DW, Deng Y, Kugathasan L, Zhang Q, Stewart DJ (2005). 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 96: 442–450.
66. Zhou L, Chen Z, Vanderslice P, So SP, Ruan KH, Willerson JT et al. (2013). Endothelial-like progenitor cells engineered to produce prostacyclin rescue monocrotaline-induced pulmonary arterial hypertension and provide right ventricle benefits. Circulation 128: 982–994.