CD13 promotes mesenchymal stem cell-mediated regeneration of ischemic muscle

Frontiers in Physiology

Volumn 4 JAN, Issue , 2014, Pages

  Rahman, M Mamunur ^a   Subramani, Jaganathan ^a,b   Ghosh, Mallika ^a   Denninger, Jiyeon K ^a   Takeda, Kotaro ^a   Fong, Guo Hua ^a   Carlson, Morgan E ^a,c   Shapiro, Linda H ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^c GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

Adhesion; CD13; Cell transplantation; Hindlimb ischemia; Mesenchymal stem cells

Indexed keywords

EID: 84893496040     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00402     Document Type: Article

References (40)

1. Armulik, A., Genove, G., and Betsholtz, C. (2011). Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215. doi: 10.1016/j.devcel.2011.07.001.
2. Aust, L., Devlin, B., Foster, S. J., Halvorsen, Y. D., Hicok, K., du Laney, T., et al. (2004). Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 6, 7-14. doi: 10.1080/14653240310004539.
3. Bhagwat, S. V., Lahdenranta, J., Giordano, R., Arap, W., Pasqualini, R., and Shapiro, L. H. (2001). CD13/APN is activated by angiogenic signals and is essential for capillary tube formation. Blood 97, 652-659. doi: 10.1182/blood.V97.3.652.
4. Bhagwat, S. V., Petrovic, N., Okamoto, Y., and Shapiro, L. H. (2003). The angiogenic regulator CD13/APN is a transcriptional target of ras signaling pathways in endothelial morphogenesis. Blood 101, 1818-1826. doi: 10.1182/blood-2002-05-1422.
5. Covas, D. T., Piccinato, C. E., Orellana, M. D., Siufi, J. L., Silva, W. A. Jr. Proto-Siqueira, R., et al. (2005). Mesenchymal stem cells can be obtained from the human saphena vein. Exp. Cell Res. 309, 340-344. doi: 10.1016/j.yexcr.2005.06.005.
6. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., et al. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. the international society for cellular therapy position statement. Cytotherapy 8, 315-317. doi: 10.1080/14653240600855905.
7. Fan, C. G., Tang, F. W., Zhang, Q. J., Lu, S. H., Liu, H. Y., Zhao, Z. M., et al. (2005). Characterization and neural differentiation of fetal lung mesenchymal stem cells. Cell Transplant. 14, 311-321. doi: 10.3727/000000005783983070.
8. Funk, P. E., Kincade, P. W., and Witte, P. L. (1994). Native associations of early hematopoietic stem cells and stromal cells isolated in bone marrow cell aggregates. Blood 83, 361-369.
9. Ghosh, M., Mcauliffe, B., Subramani, J., Basu, S., and Shapiro, L. H. (2012). CD13 regulates dendritic cell cross-presentation and T cell responses by inhibiting receptor-mediated antigen uptake. J. Immunol. 188, 5489-5499. doi: 10.4049/jimmunol.1103490.
10. Gros, C., Giros, B., and Schwartz, J. C. (1985). Identification of aminopeptidase M as an enkephalin-inactivating enzyme in rat cerebral membranes. Biochemistry 24, 2179-2185. doi: 10.1021/bi00330a011.
11. Hegde, S. P., Kumar, A., Kurschner, C., and Shapiro, L. H. (1998). c-Maf interacts with c-Myb to regulate transcription of an early myeloid gene during differentiation. Mol. Cell. Biol. 18, 2729-2737.
12. Hegde, S. P., Zhao, J., Ashmun, R. A., and Shapiro, L. H. (1999). c-Maf induces monocytic differentiation and apoptosis in bipotent myeloid progenitors. Blood 94, 1578-1589.
13. Hu, X., Wei, L., Taylor, T. M., Wei, J., Zhou, X., Wang, J. A., et al. (2011). Hypoxic preconditioning enhances bone marrow mesenchymal stem cell migration via Kv2.1 channel and FAK activation. Am. J. Physiol. Cell Physiol. 301, C362-C372. doi: 10.1152/ajpcell.00013.2010.
14. Jamur, M. C., Grodzki, A. C., Berenstein, E. H., Hamawy, M. M., Siraganian, R. P., and Oliver, C. (2005). Identification and characterization of undifferentiated mast cells in mouse bone marrow. Blood 105, 4282-4289. doi: 10.1182/blood-2004-02-0756.
15. Kim, S. W., Zhang, H. Z., Kim, C. E., An, H. S., Kim, J. M., and Kim, M. H. (2012). Amniotic mesenchymal stem cells have robust angiogenic properties and are effective in treating hindlimb ischaemia. Cardiovasc. Res. 93, 525-534. doi: 10.1093/cvr/cvr328.
16. Liao, X., Lu, S., Zhuo, Y., Winter, C., Xu, W., and Wang, Y. (2012). Visualization of Src and FAK activity during the differentiation process from HMSCs to osteoblasts. PLoS ONE 7:e42709. doi: 10.1371/journal.pone.0042709.
17. Limbourg, A., Korff, T., Napp, L. C., Schaper, W., Drexler, H., and Limbourg, F. P. (2009). Evaluation of postnatal arteriogenesis and angiogenesis in a mouse model of hind-limb ischemia. Nat. Protoc. 4, 1737-1746. doi: 10.1038/nprot.2009.185.
18. Look, A. T., Ashmun, R. A., Shapiro, L. H., and Peiper, S. C. (1989). Human myeloid plasma membrane glycoprotein CD13 (gp150) is identical to aminopeptidase N. J. Clin. Invest. 83, 1299-1307. doi: 10.1172/JCI114015.
19. Luan, Y., and Xu, W. (2007). The structure and main functions of aminopeptidase N. Curr. Med. Chem. 14, 639-647. doi: 10.2174/092986707780059571.
20. McClellan, J. B. Jr., and Garner, C. W. (1980). Purification and properties of human intestine alanine aminopeptidase. Biochim. Biophys. Acta 613, 160-167. doi: 10.1016/0005-2744(80)90202-8.
21. Meng, F., Rui, Y., Xu, L., Wan, C., Jiang, X., and Li, G. (2013). Aqp1 enhances migration of bone marrow mesenchymal stem cells through regulation of FAK and beta-catenin. Stem Cells Dev. 23, 66-75. doi: 10.1089/scd.2013.0185.
22. Mina-Osorio, P. (2008). The moonlighting enzyme CD13: old and new functions to target. Trends Mol. Med. 14, 361-371. doi: 10.1016/j.molmed.2008.06.003.
23. Mina-Osorio, P., Winnicka, B., O'Conor, C., Grant, C. L., Vogel, L. K., Rodriguez-Pinto, D., et al. (2008). CD13 is a novel mediator of monocytic/endothelial cell adhesion. J. Leukoc. Biol. 84, 448-459. doi: 10.1189/jlb.1107802.
24. Musina, R. A., Bekchanova, E. S., and Sukhikh, G. T. (2005). Comparison of mesenchymal stem cells obtained from different human tissues. Bull. Exp. Biol. Med. 139, 504-509. doi: 10.1007/s10517-005-0331-1.
25. Pasqualini, R., Koivunen, E., Kain, R., Lahdenranta, J., Sakamoto, M., Stryhn, A., et al. (2000). Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res. 60, 722-727.
26. Peister, A., Mellad, J. A., Larson, B. L., Hall, B. M., Gibson, L. F., and Prockop, D. J. (2004). Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103, 1662-1668. doi: 10.1182/blood-2003-09-3070.
27. Pereira, F. E., Cronin, C., Ghosh, M., Zhou, S. Y., Agosto, M., Subramani, J., et al. (2013). CD13 is essential for inflammatory trafficking and infarct healing following permanent coronary artery occlusion in mice. Cardiovasc. Res. 100, 74-83. doi: 10.1093/cvr/cvt155.
28. Petrovic, N., Schacke, W., Gahagan, J. R., O'Conor, C. A., Winnicka, B., Conway, R. E., et al. (2007). CD13/APN regulates endothelial invasion and filopodia formation. Blood 110, 142-150. doi: 10.1182/blood-2006-02-002931.
29. Rahman, M. M., Ghosh, M., Subramani, J., Fong, G. H., Carlson, M., and Shapiro, L. H. (2013). CD13 regulates anchorage and differentiation of the skeletal muscle satellite stem cell population in ischemic injury. Stem Cells doi: 10.1002/stem.1610. [Epub ahead of print].
30. Schulman, I. H., and Hare, J. M. (2012). Key developments in stem cell therapy in cardiology. Regen. Med. 7, 17-24. doi: 10.2217/rme.12.80.
31. Seeberger, K. L., Dufour, J. M., Shapiro, A. M., Lakey, J. R., Rajotte, R. V., and Korbutt, G. S. (2006). Expansion of mesenchymal stem cells from human pancreatic ductal epithelium. Lab. Invest. 86, 141-153. doi: 10.1038/labinvest.3700377.
32. Shipp, M. A., and Look, A. T. (1993). Hematopoietic differentiation antigens that are membrane-associated enzymes: cutting is the key! Blood 82, 1052-1070.
33. Song, H., Chang, W., Lim, S., Seo, H. S., Shim, C. Y., Park, S., et al. (2007). Tissue transglutaminase is essential for integrin-mediated survival of bone marrow-derived mesenchymal stem cells. Stem Cells 25, 1431-1438. doi: 10.1634/stemcells.2006-0467.
34. Stabile, E., Burnett, M. S., Watkins, C., Kinnaird, T., Bachis, A., la Sala, A., et al. (2003). Impaired arteriogenic response to acute hindlimb ischemia in CD4-knockout mice. Circulation 108, 205-210. doi: 10.1161/01.CIR.0000079225.50817.71.
35. Subcomittee, I.-W. N. (1984). Nomenclature for clusters of differentiation (CD) of antigens defined on human leukocyte populations. IUIS-WHO nomenclature subcommittee. Bull. World Health Organ. 62, 809-815.
36. Subramani, J., Ghosh, M., Rahman, M. M., Caromile, L. A., Gerber, C., Rezaul, M., et al. (2013). Tyrosine phosphorylation of CD13 regulates inflammatory cell-cell adhesion and monocyte trafficking. J. Immunol. 191, 3905-3912. doi: 10.4049/jimmunol.1301348.
37. Trubiani, O., di Primio, R., Traini, T., Pizzicannella, J., Scarano, A., Piattelli, A., et al. (2005). Morphological and cytofluorimetric analysis of adult mesenchymal stem cells expanded ex vivo from periodontal ligament. Int. J. Immunopathol. Pharmacol. 18, 213-221.
38. Williams, A. R., and Hare, J. M. (2011). Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ. Res. 109, 923-940. doi: 10.1161/CIRCRESAHA.111.243147.
39. Winnicka, B., O'Conor, C., Schacke, W., Vernier, K., Grant, C. L., Fenteany, F. H., et al. (2010). CD13 is dispensable for normal hematopoiesis and myeloid cell functions in the mouse. J. Leukoc. Biol. 88, 347-359. doi: 10.1189/jlb.0210065.
40. Yeager, C. L., Ashmun, R. A., Williams, R. K., Cardellichio, C. B., Shapiro, L. H., Look, A. T., et al. (1992). Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357, 420-422. doi: 10.1038/357420a0.