Adipose stem cell treatment in mice attenuates lung and systemic injury induced by cigarette smoking

American Journal of Respiratory and Critical Care Medicine

Volumn 183, Issue 2, 2011, Pages 215-225

  Schweitzer, Kelly S ^a   Johnstone, Brian H ^a   Garrison, Jana ^a   Rush, Natalia I ^a   Cooper, Scott ^a   Traktuev, Dmitry O ^a   Feng, Dongni ^a   Adamowicz, Jeremy J ^a   Van Demark, Mary ^a   Fisher, Amanda J ^a   Kamocki, Krzysztof ^a   Brown, Mary Beth ^a   Presson Jr , Robert G ^a   Broxmeyer, Hal E ^a   March, Keith L ^a   Petrache, Irina ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Cell death; Chronic obstructive; Endothelium; Human; Pulmonary disease; Regenerative medicine

Indexed keywords

CASPASE; CIGARETTE SMOKE; VASCULOTROPIN RECEPTOR;

ADIPOSE TISSUE CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FUNCTION; CIGARETTE SMOKING; ENDOTHELIUM CELL; ENZYME ACTIVATION; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; LUNG EMPHYSEMA; LUNG VOLUME; MALE; MOUSE; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; WEIGHT REDUCTION; WOUND HEALING;

ADIPOSE TISSUE; ADULT STEM CELLS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL CULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; HUMANS; INFLAMMATION; LUNG INJURY; MICE; MICE, INBRED C57BL; PULMONARY ALVEOLI; PULMONARY EMPHYSEMA; SMOKING; STEM CELL TRANSPLANTATION; TRANSPLANTATION, HETEROLOGOUS; TRANSPLANTATION, HOMOLOGOUS; WEIGHT LOSS;

EID: 77958464493     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201001-0126OC     Document Type: Article

References (46)

1. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 2000;106:1311-1319.
2. Diab KJ, Adamowicz JJ, Kamocki K, Rush NI, Garrison J, Gu Y, Schweitzer KS, Skobeleva A, Rajashekhar G, Hubbard WC, et al. Stimulation of sphingosine 1 phosphate signaling as an alveolar cell survival strategy in emphysema. Am J Respir Crit Care Med 2010;181:344-352.
3. Petrache I, Natarajan V, Zhen L, Medler TR, Richter AT, Cho C, Hubbard WC, Berdyshev EV, Tuder RM. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat Med 2005;11:491-498.
4. Giordano RJ, Lahdenranta J, Zhen L, Chukwueke U, Petrache I, Langley RR, Fidler IJ, Pasqualini R, Tuder RM, Arap W. Targeted induction of lung endothelial cell apoptosis causes emphysema-like changes in the mouse. J Biol Chem 2008;283:29447-29460.
5. Cai L, Johnstone BH, Cook TG, Liang Z, Traktuev D, Cornetta K, Ingram DA, Rosen ED, March KL. Suppression of hepatocyte growth factor production impairs the ability of adipose-derived stem cells to promote ischemic tissue revascularization. Stem Cells 2007;25:3234-3243.
6. Wei X, Du Z, Zhao L, Feng D, Wei G, He Y, Tan J, Lee WH, Hampel H, Dodel R, et al. Ifats collection: the conditioned media of adipose stromal cells protect against hypoxia-ischemia-induced brain damage in neonatal rats. Stem Cells 2009;27:478-488.
7. Ishizawa K, Kubo H, Yamada M, Kobayashi S, Numasaki M, Ueda S, Suzuki T, Sasaki H. Bone marrow-derived cells contribute to lung regeneration after elastase-induced pulmonary emphysema. FEBS Lett 2004;556:249-252.
8. Shigemura N, Okumura M, Mizuno S, Imanishi Y, Nakamura T, Sawa Y. Autologous transplantation of adipose tissue-derived stromal cells ameliorates pulmonary emphysema. Am J Transplant 2006;6:2592-2600. (Pubitemid 44571679)
9. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001;7:211-228.
10. Rehman J, Li J, Parvathaneni L, Karlsson G, Panchal VR, Temm CJ, Mahenthiran J, March KL. Exercise acutely increases circulating endothelial progenitor cells and monocyte-/macrophage-derived angiogenic cells. J Am Coll Cardiol 2004;43:2314-2318.
11. Rajashekhar G, Traktuev DO, Roell WC, Johnstone BH, Merfeld-Clauss S, Van Natta B, Rosen ED, March KL, Clauss M. Ifats collection: adipose stromal cell differentiation is reduced by endothelial cell contact and paracrine communication. Role of canonical WNT signaling. Stem Cells 2008;26:2674-2681.
12. Cai L, Johnstone BH, Cook TG, Tan J, Fishbein MC, Chen PS, March KL. Ifats collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells 2009;27:230-237.
13. Rodriguez AM, Pisani D, Dechesne CA, Turc-Carel C, Kurzenne JY, Wdziekonski B, Villageois A, Bagnis C, Breittmayer JP, Groux H, et al. Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent MDX mouse. J Exp Med 2005;201:1397-1405.
14. Wei X, Zhao L, Zhong J, Gu H, Feng D, Johnstone BH, March KL, Farlow MR, Du Y. Adipose stromal cells-secreted neuroprotective media against neuronal apoptosis. Neurosci Lett 2009;462:76-79.
15. Traktuev DO, Prater DN, Merfeld-Clauss S, Sanjeevaiah AR, Saadatzadeh MR, Murphy M, Johnstone BH, Ingram DA, March KL. Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res 2009;104:1410-1420.
16. Guerassimov A, Hoshino Y, Takubo Y, Turcotte A, Yamamoto M, Ghezzo H, Triantafillopoulos A, Whittaker K, Hoidal JR, Cosio MG. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am J Respir Crit Care Med 2004;170:974-980.
17. Bartalesi B, Cavarra E, Fineschi S, Lucattelli M, Lunghi B, Martorana PA, Lungarella G. Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. Eur Respir J 2005;25:15-22.
18. Agusti AG, Noguera A, Sauleda J, Sala E, Pons J, Busquets X. Systemic effects of chronic obstructive pulmonary disease. Eur Respir J 2003;21:347-360.
19. Oudijk EJ, Lammers JW, Koenderman L. Systemic inflammation in chronic obstructive pulmonary disease. Eur Respir J Suppl 2003;46:5s-13s.
20. Gosker HR, Langen RC, Bracke KR, Joos GF, Brusselle GG, Steele C, Ward KA, Wouters EF, Schols AM. Extrapulmonary manifestations of chronic obstructive pulmonary disease in a mouse model of chronic cigarette smoke exposure. Am J Respir Cell Mol Biol 2009;40:710-716.
21. Rabkin S, Boyko E, Streja D. Relationship of weight loss and cigarette smoking to changes in high-density lipoprotein cholesterol. Am J Clin Nutr 1981;34:1764-1768.
22. Serobyan N, Orlovskaya I, Kozlov V, Khaldoyanidi SK. Exposure to nicotine during gestation interferes with the colonization of fetal bone marrow by hematopoietic stem/progenitor cells. Stem Cells Dev 2005;14:81-91.
23. Serobyan N, Schraufstatter IU, Strongin A, Khaldoyanidi SK. Nicotinic acetylcholine receptor-mediated stimulation of endothelial cells results in the arrest of haematopoietic progenitor cells on endothelium. Br J Haematol 2005;129:257-265.
24. Traktuev DO, Merfeld-Clauss S, Li J, Kolonin M, Arap W, Pasqualini R, Johnstone BH, March KL. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res 2008;102:77-85.
25. Soriano P. Generalized lacz expression with the ROSA26 CRE reporter strain. Nat Genet 1999;21:70-71.
26. Tuder RM, Zhen L, Cho CY, Taraseviciene-Stewart L, Kasahara Y, Salvemini D, Voelkel NF, Flores SC. Oxidative stress and apoptosis interact and cause emphysema due to vascular endothelial growth factor receptor blockade. Am J Respir Cell Mol Biol 2003;29:88-97.
27. Aherne WA, Dunnill MS. Morphometry. London: E. Arnold; 1982.
28. Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, Liles WC, Li X, Graham-Evans B, Campbell TB, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 2005;201:1307-1318.
29. Cooper S, Broxmeyer HE. Current protocols in immunology. New York: John Wiley & Sons; 1996.
30. Carp H, Janoff A. Inactivation of bronchial mucous proteinase inhibitor by cigarette smoke and phagocyte-derived oxidants. Exp Lung Res 1980;1:225-237.
31. Liu X, Kohyama T, Kobayashi T, Abe S, Kim H, Reed EC, Rennard SI. Cigarette smoke extract inhibits chemotaxis and collagen gel contraction mediated by human bone marrow osteoprogenitor cells and osteoblast-like cells. Osteoporos Int 2003;14:235-242.
32. Pandit TS, Sikora L, Muralidhar G, Rao SP, Sriramarao P. Sustained exposure to nicotine leads to extramedullary hematopoiesis in the spleen. Stem Cells 2006;24:2373-2381.
33. Lee EY, Xia Y, Kim W, Kim M, Kim T, Kim K, Park B, Sung J. Hypoxia-enhanced wound-healing function of adipose-derived stem cells: increase in stem cell proliferation and up-regulation of VEGF and BFGF. Wound Repair Regen 2009;17:540-547.
34. Wang JH, Liu N, Du HW, Weng JS, Chen RH, Xiao YC, Zhang YX. Effects of adipose-derived stem cell transplantation on the angiogenesis and the expression of BFGF and VEGF in the brain post focal cerebral ischemia in rats [in Chinese]. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 2008;24:958-961.
35. Moy AB, Van Engelenhoven J, Bodmer J, Kamath J, Keese C, Giaever I, Shasby S, Shasby DM. Histamine and thrombin modulate endothelial focal adhesion through centripetal and centrifugal forces. J Clin Invest 1996;97:1020-1027.
36. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S. Genetic ablation of NRF2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 2004;114:1248-1259.
37. Kang MJ, Lee CG, Cho SJ, Homer RJ, Elias JA. IFN-gamma-dependent DNA injury and/or apoptosis are critical in cigarette smoke-induced murine emphysema. Proc Am Thorac Soc 2006;3:517-518.
38. Hoffman AM, Shifren A, Mazan MR, Gruntman AM, Lascola KM, Nolen-Walston R, Kim CF, Tsai L, Pierce RA, Mecham RP, et al. Matrix modulation of compensatory lung regrowth and progenitor cell proliferation in mice. Am J Physiol Lung Cell Mol Physiol 2010;298:L158-L168.
39. Hegab AE, Kubo H, Yamaya M, Asada M, He M, Fujino N, Mizuno S, Nakamura T. Intranasal HGF administration ameliorates the physiologic and morphologic changes in lung emphysema. Mol Ther 2008;16:1417-1426.
40. Shigemura N, Okumura M, Mizuno S, Imanishi Y, Matsuyama A, Shiono H, Nakamura T, Sawa Y. Lung tissue engineering technique with adipose stromal cells improves surgical outcome for pulmonary emphysema. Am J Respir Crit Care Med 2006;174:1199-1205.
41. Zhao Y, Ohkawara H, Rehman J, Wary K, Vogel S, Minshall R, Zhao Y, Malik A. Bone marrow progenitor cells induce endothelial adherens junction integrity by sphingosine-1-phosphate-mediated RAC1 and CDC42 signaling. Circ Res 2009;105:696-704.
42. Di Francia M, Barbier D, Mege JL, Orehek J. Tumor necrosis factor-alpha levels and weight loss in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1994;150:1453-1455.
43. Gimble J, Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 2003;5:362-369.
44. Aust L, Devlin B, Foster SJ, Halvorsen YD, Hicok K, du Laney T, Sen A, Willingmyre GD, Gimble JM. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 2004;6:7-14.
45. Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, Semprun-Prieto L, Delafontaine P, Prockop DJ. Intravenous HMSCS improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009;5:54-63.
46. Van Eeden S, Yeung A, Quinlam K, Hogg JC. Systemic response to ambient particulate matter relevance to chronic obstructive pulmonary disease. Proc Am Thorac Soc 2005;2:61-67.