Lung-derived mesenchymal stromal cell post-transplantation survival, persistence, paracrine expression, and repair of elastase-injured lung

Stem Cells and Development

Volumn 20, Issue 10, 2011, Pages 1779-1792

  Hoffman, Andrew M ^a   Paxson, Julia A ^a   Mazan, Melissa R ^a   Davis, Airiel M ^a   Tyagi, Shivraj ^b   Murthy, Shankar ^b   Ingenito, Edward P ^b  

^a TUFTS UNIVERSITY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALPHA2 INTEGRIN; CD45 ANTIGEN; CXCL2 CHEMOKINE; ELASTASE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 11; INTERLEUKIN 6; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; SCATTER FACTOR; SOMATOMEDIN B; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CCL2; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW MESENCHYMAL STROMAL CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL SURVIVAL; CELL TRANSPLANTATION; CLONOGENESIS; CONTROLLED STUDY; EMPHYSEMA; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE EXPRESSION; LUNG ALVEOLUS CELL; LUNG MESENCHYMAL STROMAL CELL; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PARACRINE SIGNALING; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL;

ANIMALS; BONE MARROW CELLS; CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; LUNG; LUNG INJURY; MALE; MEMBRANE PROTEINS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MULTIPOTENT STEM CELLS; PANCREATIC ELASTASE; PARACRINE COMMUNICATION; SURVIVAL ANALYSIS; WOUND HEALING;

EID: 80053401510     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0105     Document Type: Article

References (64)

1. da Silva Meirelles L, PC Chagastelles and NB Nardi. (2006). Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204-2213. (Pubitemid 43960310)
2. Weiss DJ, JK Kolls, LA Ortiz, A Panoskaltsis-Mortari and DJ Prockop. (2008). Stem cells and cell therapies in lung biology and lung diseases. Proc Am Thorac Soc 5:637-667. (Pubitemid 352031537)
3. Matthay MA, A Goolaerts, JP Howard and JW Lee. (2010). Mesenchymal stem cells for acute lung injury: preclinical evidence. Crit Care Med 38:S569-S573.
4. Zhen G, Z Xue, J Zhao, N Gu, Z Tang, Y Xu and Z Zhang. (2010). Mesenchymal stem cell transplantation increases expression of vascular endothelial growth factor in papaininduced emphysematous lungs and inhibits apoptosis of lung cells. Cytotherapy 12:605-614.
5. Shigemura N, M Okumura, S Mizuno, Y Imanishi, T Nakamura and Y Sawa. (2006). Autologous transplantation ofadipose tissue-derived stromal cells ameliorates pulmonary emphysema. Am J Transplant 6:2592-2600. (Pubitemid 44571679)
6. Ishizawa K, H Kubo, M Yamada, S Kobayashi, M Numasaki, S Ueda, T Suzuki and H Sasaki. (2004). Bone marrowderived cells contribute to lung regeneration after elastaseinduced pulmonary emphysema. FEBS Lett 556:249-252. (Pubitemid 38058587)
7. Katsha AM, S Ohkouchi, H Xin, M Kanehira, R Sun, T Nukiwa and Y Saijo. (2011). Paracrine factors of multipotent stromal cells ameliorate lung injury in an elastase-induced emphysema model. Mol Ther 19:196-203.
8. Nemeth K, A Leelahavanichkul, PS Yuen, B Mayer, A Parmelee, K Doi, PG Robey, K Leelahavanichkul, BH Koller, 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.
9. Xu J, J Qu, L Cao, Y Sai, C Chen, L He and L Yu. (2008). Mesenchymal stem cell-based angiopoietin-1 gene therapy for acute lung injury induced by lipopolysaccharide in mice. J Pathol 214:472-481. (Pubitemid 351340567)
10. Krasnodembskaya A, Y Song, X Fang, N Gupta, V Serikov, JW Lee and MA Matthay. (2010). Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37. Stem Cells 28:2229-2238.
11. Serikov VB, VM Mikhaylov, AD Krasnodembskay and MA Matthay. (2008). Bone marrow-derived cells participate in stromal remodeling of the lung following acute bacterial pneumonia in mice. Lung 186:179-190.
12. van Haaften T, R Byrne, S Bonnet, GY Rochefort, J Akabutu, M Bouchentouf, GJ Rey-Parra, J Galipeau, A Haromy, et al. (2009). Airway delivery of mesenchymal stem cells prevents arrested alveolar growth in neonatal lung injury in rats. Am J Respir Crit Care Med 180:1131-1142.
13. Aslam M, R Baveja, OD Liang, A Fernandez-Gonzalez, C Lee, SA Mitsialis and S Kourembanas. (2009). Bone marrow stromal cells attenuate lung injury in a murine model of neonatal chronic lung disease. Am J Respir Crit Care Med 180:1122-1130.
14. Fritzell JA Jr., Q Mao, S Gundavarapu, T Pasquariello, JM Aliotta, A Ayala, JF Padbury and ME De Paepe. (2009). Fate and effects of adult bone marrow cells in lungs of normoxic and hyperoxic newborn mice. Am J Respir Cell Mol Biol 40:575-587.
15. Tian ZF, J Du, XM Fu, B Wang, XY Hong and ZC Feng. (2008). Influence of human bone marrow-derived mesenchymal stem cells on the lung of newborn rats damaged by hyperoxia. Zhonghua Er Ke Za Zhi 46:4-8.
16. Tian ZF, J Du, B Wang, XY Hong and ZC Feng. (2007). Intravenous infusion of rat bone marrow-derived mesenchymal stem cells ameliorates hyperoxia-induced lung injury in neonatal rats. Nan Fang Yi Ke Da Xue Xue Bao 27:1692-1695.
17. Irwin D, K Helm, N Campbell, M Imamura, K Fagan, J Harral, M Carr, KA Young, D Klemm, et al. (2007). Neonatal lung side population cells demonstrate endothelial potential and are altered in response to hyperoxia-induced lung simplification. Am J Physiol Lung Cell Mol Physiol 293:L941-L951. (Pubitemid 47572242)
18. Lee SH, AS Jang, YE Kim, JY Cha, TH Kim, S Jung, SK Park, YK Lee, JH Won, YH Kim and CS Park. (2010). Modulation of cytokine and nitric oxide by mesenchymal stem cell transfer in lung injury/fibrosis. Respir Res 11:16.
19. Xu J, ET Gonzalez, SS Iyer, V Mac, AL Mora, RL Sutliff, A Reed, KL Brigham, P Kelly and M Rojas. (2009). Use of senescence-accelerated mouse model in bleomycin-induced lung injury suggests that bone marrow-derived cells can alter the outcome of lung injury in aged mice. J Gerontol A Biol Sci Med Sci 64:731-739.
20. Liebler JM, C Lutzko, A Banfalvi, D Senadheera, N Aghamohammadi, ED Crandall and Z Borok. (2008). Retention of human bone marrow-derived cells in murine lungs following bleomycin-induced lung injury. Am J Physiol Lung Cell Mol Physiol 295:L285-L292.
21. Cui A, HP Dai, JW Dai, BS Pang, SJ Niu, YP Lu and C Wang. (2007). Effects of bone marrow mesenchymal stem cells on bleomycin induced pulmonary fibrosis in rats. Zhonghua Jie He He Hu Xi Za Zhi 30:677-682.
22. Ortiz LA, F Gambelli, C McBride, D Gaupp, M Baddoo, N Kaminski and DG Phinney. (2003). Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 100:8407-8411. (Pubitemid 36842558)
23. McQualter JL, N Brouard, B Williams, BN Baird, S Sims- Lucas, K Yuen, SK Nilsson, PJ Simmons and I Bertoncello. (2009). Endogenous fibroblastic progenitor cells in the adult mouse lung are highly enriched in the sca-1 positive cell fraction. Stem Cells 27:623-633.
24. Summer R, K Fitzsimmons, D Dwyer, J Murphy and A Fine. (2007). Isolation of an adult mouse lung mesenchymal progenitor cell population. Am J Respir Cell Mol Biol 37:152-159. (Pubitemid 47254998)
25. Hegab AE, H Kubo, N Fujino, T Suzuki, M He, H Kato and M Yamaya. (2010). Isolation and characterization of murine multipotent lung stem cells. Stem Cells Dev 19:523-536.
26. Reynolds SD, H Shen, PR Reynolds, T Betsuyaku, JM Pilewski, F Gambelli, M DeGuiseppe, LA Ortiz and BR Stripp. (2007). Molecular and functional properties of lung SP cells. Am J Physiol Lung Cell Mol Physiol 292:L972-L983. (Pubitemid 46608244)
27. Martin J, K Helm, P Ruegg, M Varella-Garcia, E Burnham and S Majka. (2008). Adult lung side population cells have mesenchymal stem cell potential. Cytotherapy 10:140-151.
28. Jarvinen L, L Badri, S Wettlaufer, T Ohtsuka, TJ Standiford, GB Toews, DJ Pinsky, M Peters-Golden and VN Lama. (2008). Lung resident mesenchymal stem cells isolated from human lung allografts inhibit T cell proliferation via a soluble mediator. J Immunol 181:4389-4396.
29. Lama VN, L Smith, L Badri, A Flint, AC Andrei, S Murray, Z Wang, H Liao, GB Toews, et al. (2007). Evidence for tissueresident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J Clin Invest 117:989-996. (Pubitemid 46556755)
30. Hennrick KT, AG Keeton, S Nanua, TG Kijek, AM Goldsmith, US Sajjan, JK Bentley, VN Lama, BB Moore, et al. (2007). Lung cells from neonates show a mesenchymal stem cell phenotype. Am J Respir Crit Care Med 175:1158-1164. (Pubitemid 46855457)
31. Ingenito EP, E Sen, LW Tsai, S Murthy and A Hoffman. (2010). Design and testing of biological scaffolds for delivering reparative cells to target sites in the lung. J Tissue Eng Regen Med 4:259-272.
32. Ingenito EP, L Tsai, S Murthy, S Tyagi, M Mazan and A Hoffman. (2011). Autologous lung-derived mesenchymal stem cell transplantation in experimental emphysema. Cell Transplant DOI: 10.3727/096368910X550233.
33. Summer R and A Fine. (2008). Mesenchymal progenitor cell research: limitations and recommendations. Proc Am Thorac Soc 5:707-710.
34. Jun DH, C Garat, J West, N Thorn, KS Chow, T Cleaver, T Sullivan, EC Torchia, C Childs, et al. (2011). The pathology of bleomycin induced fibrosis is associated with loss ofresident lung mesenchymal stem cells which regulate effector t-cell proliferation. Stem Cells 29:725-735.
35. Ingenito EP, E Sen, LW Tsai, S Murthy and A Hoffman. (2009). Design and testing of biological scaffolds for delivering reparative cells to target sites in the lung. J Tissue Eng Regen Med 4:259-272.
36. Hoffman AM, A Shifren, MR Mazan, AM Gruntman, KM Lascola, RD Nolen-Walston, CF Kim, L Tsai, RA Pierce, RP Mecham and EP Ingenito. (2010). Matrix modulation of compensatory lung regrowth and progenitor cell proliferation in mice. Am J Physiol Lung Cell Mol Physiol 298:L158-L168.
37. Paxson JA, CD Parkin, LK Iyer, MR Mazan, EP Ingenito and AM Hoffman. (2009). Global gene expression patterns in the post-pneumonectomy lung of adult mice. Respir Res 10:92.
38. Pfaffl MW. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
39. Xouri G and S Christian. (2010). Origin and function of tumor stroma fibroblasts. Semin Cell Dev Biol 21:40-46.
40. Sabeh F, XY Li, TL Saunders, RG Rowe and SJ Weiss. (2009). Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J Biol Chem 284:23001-23011.
41. Haniffa MA, MP Collin, CD Buckley and F Dazzi. (2009). Mesenchymal stem cells: the fibroblasts' new clothes? Haematologica 94:258-263.
42. Haniffa MA, XN Wang, U Holtick, M Rae, JD Isaacs, AM Dickinson, CM Hilkens and MP Collin. (2007). Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J Immunol 179:1595-1604.
43. Sabatini F, L Petecchia, M Tavian, V Jodon de Villeroche, GA Rossi and D Brouty-Boye. (2005). Human bronchial fibroblasts exhibit a mesenchymal stem cell phenotype and multilineage differentiating potentialities. Lab Invest 85:962-971. (Pubitemid 41486421)
44. McQualter JL, N Brouard, B Williams, BN Baird, S Sims- Lucas, K Yuen, SK Nilsson, PJ Simmons and I Bertoncello. (2009). Endogenous fibroblastic progenitor cells in the adult mouse lung are highly enriched in the Sca-1 positive cell fraction. Stem Cells 27:623-633.
45. Weiss DJ, MA Berberich, Z Borok, DB Gail, JK Kolls, C Penland and DJ Prockop. (2006). Adult stem cells, lung biology, and lung disease. NHLBI/Cystic Fibrosis Foundation Workshop. Proc Am Thorac Soc 3:193-207. (Pubitemid 43668182)
46. Hayflick L. (1965). The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37:614-636.
47. Balber AE. (2011). ALDH bright stem and progenitor cell populations from normal tissues: characteristics, activities and emerging uses in regenerative medicine. Stem Cells 29:570-575.
48. Lee CH, B Shah, EK Moioli and JJ Mao. (2010). CTGF directs fibroblast differentiation from human mesenchymal stem/ stromal cells and defines connective tissue healing in a rodent injury model. J Clin Invest 120:3340-3349.
49. Petersen TH, EA Calle, L Zhao, EJ Lee, L Gui, MB Raredon, K Gavrilov, T Yi, ZW Zhuang, et al. (2010). Tissueengineered lungs for in vivo implantation. Science 329:538-541.
50. Cortiella J, J Niles, A Cantu, A Brettler, A Pham, G Vargas, S Winston, J Wang, S Walls and JE Nichols. (2010). Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng Part A 16:2565-2580.
51. Karp JM and GS Leng Teo. (2009). Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4:206-216.
52. Sordi V. (2009). Mesenchymal stem cell homing capacity. Transplantation 87:S42-S45.
53. Lochter A, M Navre, Z Werb and MJ Bissell. (1999). alpha1 and alpha2 integrins mediate invasive activity of mouse mammary carcinoma cells through regulation of stromelysin- 1 expression. Mol Biol Cell 10:271-282. (Pubitemid 29156472)
54. Pankov R, Y Endo, S Even-Ram, M Araki, K Clark, E Cukierman, K Matsumoto and KM Yamada. (2005). A Rac switch regulates random versus directionally persistent cell migration. J Cell Biol 170:793-802. (Pubitemid 41242111)
55. Schmidt S and P Friedl. (2010). Interstitial cell migration: integrin-dependent and alternative adhesion mechanisms. Cell Tissue Res 339:83-92.
56. Kollar K, MM Cook, K Atkinson and G Brooke. (2009). Molecular mechanisms involved in mesenchymal stem cell migration to the site of acute myocardial infarction. Int J Cell Biol 2009:904682.
57. Petrie RJ, AD Doyle and KM Yamada. (2009). Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 10:538-549.
58. Epting CL, JE Lopez, A Pedersen, C Brown, P Spitz, PC Ursell and HS Bernstein. (2008). Stem cell antigen-1 regulates the tempo of muscle repair through effects on proliferation of alpha7 integrin-expressing myoblasts. Exp Cell Res 314:1125-1135.
59. Sudo K, Y Yamada, K Saito, S Shimizu, H Ohashi, T Kato, H Moriwaki, H Ito and M Seishima. (2008). TNF-alpha and IL- 6 signals from the bone marrow derived cells are necessary for normal murine liver regeneration. Biochim Biophys Acta 1782:671-679.
60. Pachowka M, J Zegarska, R Ciecierski and G Korczak- Kowalska. (2008). The role of IL-6 during the late phase of liver regeneration. Ann Transplant 13:15-19.
61. Nechemia-Arbely Y, A Shriki, U Denz, C Drucker, J Scheller, J Raub, O Pappo, S Rose-John, E Galun and JH Axelrod. (2011). Early hepatocyte DNA synthetic response posthepatectomy is modulated by IL-6 trans-signaling and PI3K/AKT activation. J Hepatol 54:922-929.
62. Sun R, B Jaruga, S Kulkarni, H Sun and B Gao. (2005). IL-6 modulates hepatocyte proliferation via induction of HGF/ p21cip1: regulation by SOCS3. Biochem Biophys Res Commun 338:1943-1949. (Pubitemid 41643111)
63. Cai L, BH Johnstone, TG Cook, Z Liang, D Traktuev, K Cornetta, DA Ingram, ED Rosen and KL March. (2007). Suppression of hepatocyte growth factor production impairs the ability of adipose-derived stem cells to promote ischemic tissue revascularization. Stem Cells 25:3234-3243. (Pubitemid 350294449)
64. Matthay MA, BT Thompson, EJ Read, DH McKenna Jr., KD Liu, CS Calfee and JW Lee. (2010). Therapeutic potential of mesenchymal stem cells for severe acute lung injury. Chest 138:965-972.