Allogeneic human mesenchymal stem cells restore epithelial protein permeability in cultured human alveolar type II cells by secretion of angiopoietin-1
Xiaohui Fang, Arne P Neyrinck, Michael A Matthay, Jae W Lee, Xiaohui Fang, Arne P Neyrinck, Michael A Matthay, Jae W Lee
Abstract
Acute lung injury is characterized by injury to the lung epithelium that leads to impaired resolution of pulmonary edema and also facilitates accumulation of protein-rich edema fluid and inflammatory cells in the distal airspaces of the lung. Recent in vivo and in vitro studies suggest that mesenchymal stem cells (MSC) may have therapeutic value for the treatment of acute lung injury. Here we tested the ability of human allogeneic mesenchymal stem cells to restore epithelial permeability to protein across primary cultures of polarized human alveolar epithelial type II cells after an inflammatory insult. Alveolar epithelial type II cells were grown on a Transwell plate with an air-liquid interface and injured by cytomix, a combination of IL-1beta, TNFalpha, and IFNgamma. Protein permeability measured by (131)I-labeled albumin flux was increased by 5-fold over 24 h after cytokine-induced injury. Co-culture of human MSC restored type II cell epithelial permeability to protein to control levels. Using siRNA knockdown of potential paracrine soluble factors, we found that angiopoietin-1 secretion was responsible for this beneficial effect in part by preventing actin stress fiber formation and claudin 18 disorganization through suppression of NFkappaB activity. This study provides novel evidence for a beneficial effect of MSC on alveolar epithelial permeability to protein.
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References
- Rubenfeld G. D., Caldwell E., Peabody E., Weaver J., Martin D. P., Neff M., Stern E. J., Hudson L. D. (2005) N. Engl. J. Med. 353, 1685–1693
- The Acute Respiratory Distress Syndrome Network (2000) N. Engl. J. Med. 342, 1301–1308
- Wiedemann H. P., Wheeler A. P., Bernard G. R., Thompson B. T., Hayden D., deBoisblanc B., Connors A. F., Jr., Hite R. D., Harabin A. L. (2006) N. Engl. J. Med. 354, 2564–2575
- Ware L. B., Matthay M. A. (2000) N. Engl. J. Med. 342, 1334–1349
- Ware L. B., Matthay M. A. (2001) Am. J. Respir. Crit. Care Med. 163, 1376–1383
- Krause D. S., Theise N. D., Collector M. I., Henegariu O., Hwang S., Gardner R., Neutzel S., Sharkis S. J. (2001) Cell 105, 369–377
- Wang G., Bunnell B. A., Painter R. G., Quiniones B. C., Tom S., Lanson N. A., Jr., Spees J. L., Bertucci D., Peister A., Weiss D. J., Valentine V. G., Prockop D. J., Kolls J. K. (2005) Proc. Natl. Acad. Sci. U.S.A. 102, 186–191
- Spees J. L., Pociask D. A., Sullivan D. E., Whitney M. J., Lasky J. A., Prockop D. J., Brody A. R. (2007) Am. J. Respir. Crit. Care Med. 176, 385–394
- Hung S. C., Pochampally R. R., Hsu S. C., Sanchez C., Chen S. C., Spees J., Prockop D. J. (2007) PLoS One 2, e416.
- Le Blanc K., Tammik C., Rosendahl K., Zetterberg E., Ringdén O. (2003) Exp. Hematol. 31, 890–896
- Aggarwal S., Pittenger M. F. (2005) Blood 105, 1815–1822
- Glennie S., Soeiro I., Dyson P. J., Lam E. W., Dazzi F. (2005) Blood 105, 2821–2827
- Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P. D., Matteucci P., Grisanti S., Gianni A. M. (2002) Blood 99, 3838–3843
- Klyushnenkova E., Mosca J. D., Zernetkina V., Majumdar M. K., Beggs K. J., Simonetti D. W., Deans R. J., McIntosh K. R. (2005) J. Biomed. Sci. 12, 47–57
- Chen L., Tredget E. E., Wu P. Y., Wu Y. (2008) PLoS One 3, e1886.
- Zhen G., Liu H., Gu N., Zhang H., Xu Y., Zhang Z. (2008) Front. Biosci. 13, 3415–3422
- Yamada M., Kubo H., Kobayashi S., Ishizawa K., Numasaki M., Ueda S., Suzuki T., Sasaki H. (2004) J. Immunol. 172, 1266–1272
- Xu J., Woods C. R., Mora A. L., Joodi R., Brigham K. L., Iyer S., Rojas M. (2007) Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L131–L141
- Xu J., Qu J., Cao L., Sai Y., Chen C., He L., Yu L. (2008) J. Pathol. 214, 472–481
- Weiss D. J., Kolls J. K., Ortiz L. A., Panoskaltsis-Mortari A., Prockop D. J. (2008) Proc. Am. Thorac. Soc. 5, 637–667
- Rojas M., Xu J., Woods C. R., Mora A. L., Spears W., Roman J., Brigham K. L. (2005) Am. J. Respir. Cell Mol. Biol. 33, 145–152
- Prockop D. J., Olson S. D. (2007) Blood 109, 3147–3151
- Ortiz L. A., Gambelli F., McBride C., Gaupp D., Baddoo M., Kaminski N., Phinney D. G. (2003) Proc. Natl. Acad. Sci. U.S.A. 100, 8407–8411
- Ortiz L. A., Dutreil M., Fattman C., Pandey A. C., Torres G., Go K., Phinney D. G. (2007) Proc. Natl. Acad. Sci. U.S.A. 104, 11002–11007
- Mei S. H., McCarter S. D., Deng Y., Parker C. H., Liles W. C., Stewart D. J. (2007) PLoS Med. 4, e269.
- Gupta N., Su X., Popov B., Lee J. W., Serikov V., Matthay M. A. (2007) J. Immunol. 179, 1855–1863
- Lee J. W., Fang X., Gupta N., Serikov V., Matthay M. A. (2009) Proc. Natl. Acad. Sci. U.S.A. 106, 16357–16362
- Kwak H. J., So J. N., Lee S. J., Kim I., Koh G. Y. (1999) FEBS Lett. 448, 249–253
- Thurston G., Rudge J. S., Ioffe E., Zhou H., Ross L., Croll S. D., Glazer N., Holash J., McDonald D. M., Yancopoulos G. D. (2000) Nat. Med. 6, 460–463
- Pizurki L., Zhou Z., Glynos K., Roussos C., Papapetropoulos A. (2003) Br. J. Pharmacol 139, 329–336
- Kim I., Moon S. O., Park S. K., Chae S. W., Koh G. Y. (2001) Circ. Res. 89, 477–479
- Gamble J. R., Drew J., Trezise L., Underwood A., Parsons M., Kasminkas L., Rudge J., Yancopoulos G., Vadas M. A. (2000) Circ. Res. 87, 603–607
- McCarter S. D., Mei S. H., Lai P. F., Zhang Q. W., Parker C. H., Suen R. S., Hood R. D., Zhao Y. D., Deng Y., Han R. N., Dumont D. J., Stewart D. J. (2007) Am. J. Respir. Crit. Care Med. 175, 1014–1026
- Lee J. W., Fang X., Dolganov G., Fremont R. D., Bastarache J. A., Ware L. B., Matthay M. A. (2007) J. Biol. Chem. 282, 24109–24119
- Suri C., Jones P. F., Patan S., Bartunkova S., Maisonpierre P. C., Davis S., Sato T. N., Yancopoulos G. D. (1996) Cell 87, 1171–1180
- Mammoto T., Parikh S. M., Mammoto A., Gallagher D., Chan B., Mostoslavsky G., Ingber D. E., Sukhatme V. P. (2007) J. Biol. Chem. 282, 23910–23918
- Kotton D. N., Summer R., Fine A. (2004) Exp. Hematol. 32, 340–343
- Liebler J. M., Lutzko C., Banfalvi A., Senadheera D., Aghamohammadi N., Crandall E. D., Borok Z. (2008) Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L285–L292
- Xu J., Mora A., Shim H., Stecenko A., Brigham K. L., Rojas M. (2007) Am. J. Respir. Cell Mol. Biol. 37, 291–299
- Németh K., Leelahavanichkul A., Yuen P. S., Mayer B., Parmelee A., Doi K., Robey P. G., Leelahavanichkul K., Koller B. H., Brown J. M., Hu X., Jelinek I., Star R. A., Mezey E. (2009) Nat. Med. 15, 42–49
- Caplan A. I., Dennis J. E. (2006) J. Cell. Biochem. 98, 1076–1084
- Thurston G. (2003) Cell Tissue Res. 314, 61–68
- Dumont D. J., Gradwohl G., Fong G. H., Puri M. C., Gertsenstein M., Auerbach A., Breitman M. L. (1994) Genes Dev. 8, 1897–1909
- Davis S., Aldrich T. H., Jones P. F., Acheson A., Compton D. L., Jain V., Ryan T. E., Bruno J., Radziejewski C., Maisonpierre P. C., Yancopoulos G. D. (1996) Cell 87, 1161–1169
- Maisonpierre P. C., Suri C., Jones P. F., Bartunkova S., Wiegand S. J., Radziejewski C., Compton D., McClain J., Aldrich T. H., Papadopoulos N., Daly T. J., Davis S., Sato T. N., Yancopoulos G. D. (1997) Science 277, 55–60
- Wong A. L., Haroon Z. A., Werner S., Dewhirst M. W., Greenberg C. S., Peters K. G. (1997) Circ. Res. 81, 567–574
- Wang Y., Pampou S., Fujikawa K., Varticovski L. (2004) J. Cell Physiol. 198, 53–61
- Witzenbichler B., Westermann D., Knueppel S., Schultheiss H. P., Tschope C. (2005) Circulation 111, 97–105
- Fiedler U., Reiss Y., Scharpfenecker M., Grunow V., Koidl S., Thurston G., Gale N. W., Witzenrath M., Rosseau S., Suttorp N., Sobke A., Herrmann M., Preissner K. T., Vajkoczy P., Augustin H. G. (2006) Nat. Med. 12, 235–239
- Karmpaliotis D., Kosmidou I., Ingenito E. P., Hong K., Malhotra A., Sunday M. E., Haley K. J. (2002) Am. J. Physiol. Lung Cell. Mol. Physiol. 283, L585–L595
- Harhaj N. S., Antonetti D. A. (2004) Int. J. Biochem. Cell Biol. 36, 1206–1237
- Turner J. R., Rill B. K., Carlson S. L., Carnes D., Kerner R., Mrsny R. J., Madara J. L. (1997) Am. J. Physiol. 273, C1378–C1385
- Wray C., Mao Y., Pan J., Chandrasena A., Piasta F., Frank J. A. (2009) Am. J. Physiol. Lung Cell. Mol. Physiol. 297, L219–L227
- Koval M., Ward C., Findley M. K., Roser-Page S., Helms M. N., Roman J. (2010) Am. J. Respir. Cell Mol. Biol. 42, 172–180
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