Human mesenchymal stem cells generate a distinct pericellular zone of MMP activities via binding of MMPs and secretion of high levels of TIMPs

Matrix Biology

Volumn 34, Issue , 2014, Pages 132-143

  Lozito, Thomas P ^a   Jackson, Wesley M ^b   Nesti, Leon J ^b,c,d   Tuan, Rocky S ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c WALTER REED ARMY MEDICAL CENTER   (United States)

^d Uniformed Services University of the Health Sciences   (United States)

Author keywords

Matrix metalloprotease (MMP); Mesenchymal stem cells (MSCs); Tissue inhibitors of metalloprotease (TIMP)

Indexed keywords

COLLAGENASE 3; GELATINASE A; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TISSUE INHIBITOR OF METALLOPROTEINASE 4; ENZYME PRECURSOR; GELATINASE; PROGELATINASE; PROTEIN BINDING; TISSUE INHIBITOR OF METALLOPROTEINASE-4;

ADIPOSE DERIVED STEM CELL; ARTICLE; CELL ISOLATION; CELL REGENERATION; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME RELEASE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; CELL CULTURE; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; TUMOR MICROENVIRONMENT;

CELLS, CULTURED; CELLULAR MICROENVIRONMENT; ENZYME PRECURSORS; GELATINASES; HUMANS; MATRIX METALLOPROTEINASE 13; MESENCHYMAL STROMAL CELLS; PROTEIN BINDING; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TISSUE INHIBITOR OF METALLOPROTEINASES;

EID: 84900318730     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.10.003     Document Type: Article

References (53)

1. Annabi B., Lee Y.T., Turcotte S., Naud E., Desrosiers R.R., Champagne M., Eliopoulos N., Galipeau J., Beliveau R. Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Stem Cells 2003, 21:337-347.
2. Belema-Bedada F., Uchida S., Martire A., Kostin S., Braun T. Efficient homing of multipotent adult mesenchymal stem cells depends on FROUNT-mediated clustering of CCR2. Cell Stem Cell 2008, 2:566-575.
3. Bigg H.F., Morrison C.J., Butler G.S., Bogoyevitch M.A., Wang Z., Soloway P.D., Overall C.M. Tissue inhibitor of metalloproteinases-4 inhibits but does not support the activation of gelatinase A via efficient inhibition of membrane type 1-matrix metalloproteinase. Cancer Res. 2001, 61:3610-3618.
4. Brew K., Dinakarpandian D., Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim. Biophys. Acta 2000, 1477:267-283.
5. Caplan A.I. Mesenchymal stem cells. J. Orthop. Res. 1991, 9:641-650.
6. Cotsarelis G., Sun T.T., Lavker R.M. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 1990, 61:1329-1337.
7. Coussens L.M., Tinkle C.L., Hanahan D., Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000, 103:481-490.
8. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., Andriolo G., Sun B., Zheng B., Zhang L., Norotte C., Teng P.N., Traas J., Schugar R., Deasy B.M., Badylak S., Buhring H.J., Giacobino J.P., Lazzari L., Huard J., Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
9. De Bari C., Dell'Accio F., Tylzanowski P., Luyten F.P. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001, 44:1928-1942.
10. De Becker A., Van Hummelen P., Bakkus M., Vande Broek I., De Wever J., De Waele M., Van Riet I. Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3. Haematologica 2007, 92:440-449.
11. D'Ippolito G., Diabira S., Howard G.A., Menei P., Roos B.A., Schiller P.C. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J. Cell Sci. 2004, 117:2971-2981.
12. Djouad F., Bony C., Haupl T., Uze G., Lahlou N., Louis-Plence P., Apparailly F., Canovas F., Reme T., Sany J., Jorgensen C., Noel D. Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Res. Ther. 2005, 7:R1304-R1315.
13. Emmert-Buck M.R., Emonard H.P., Corcoran M.L., Krutzsch H.C., Foidart J.M., Stetler-Stevenson W.G. Cell surface binding of TIMP-2 and pro-MMP-2/TIMP-2 complex. FEBS Lett. 1995, 364:28-32.
14. Friedenstein A.J., Petrakova K.V., Kurolesova A.I., Frolova G.P. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968, 6:230-247.
15. Friedenstein A.J., Chailakhjan R.K., Lalykina K.S. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970, 3:393-403.
16. Friedenstein A.J., Chailakhyan R.K., Gerasimov U.V. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet. 1987, 20:263-272.
17. Gronthos S., Zannettino A.C., Hay S.J., Shi S., Graves S.E., Kortesidis A., Simmons P.J. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J. Cell Sci. 2003, 116:1827-1835.
18. Gruber R., Kandler B., Holzmann P., Vogele-Kadletz M., Losert U., Fischer M.B., Watzek G. Bone marrow stromal cells can provide a local environment that favors migration and formation of tubular structures of endothelial cells. Tissue Eng. 2005, 11:896-903.
19. Hernandez-Barrantes S., Toth M., Bernardo M.M., Yurkova M., Gervasi D.C., Raz Y., Sang Q.A., Fridman R. Binding of active (57kDa) membrane type 1-matrix metalloproteinase (MT1-MMP) to tissue inhibitor of metalloproteinase (TIMP)-2 regulates MT1-MMP processing and pro-MMP-2 activation. J. Biol. Chem. 2000, 275:12080-12089.
20. Hiraoka K., Grogan S., Olee T., Lotz M. Mesenchymal progenitor cells in adult human articular cartilage. Biorheology 2006, 43:447-454.
21. Horwitz E.M., Le Blanc K., Dominici M., Mueller I., Slaper-Cortenbach I., Marini F.C., Deans R.J., Krause D.S., Keating A. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005, 7:393-395.
22. Ikejiri M., Bernardo M.M., Bonfil R.D., Toth M., Chang M., Fridman R., Mobashery S. Potent mechanism-based inhibitors for matrix metalloproteinases. J. Biol. Chem. 2005, 280:33992-34002.
23. Jackson W.M., Lozito T.P., Djouad F., Kuhn N.Z., Nesti L.J., Tuan R.S. Differentiation and regeneration potential of mesenchymal progenitor cells derived from traumatized muscle tissue. J. Cell. Mol. Med. 2011, 15:2377-2388.
24. Janjanin S., Djouad F., Shanti R.M., Baksh D., Gollapudi K., Prgomet D., Rackwitz L., Joshi A.S., Tuan R.S. Human palatine tonsil: a new potential tissue source of multipotent mesenchymal progenitor cells. Arthritis Res. Ther. 2008, 10:R83.
25. Jones E., McGonagle D. Human bone marrow mesenchymal stem cells in vivo. Rheumatology (Oxford) 2008, 47:126-131.
26. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 2003, 3:422-433.
27. Knauper V., Will H., Lopez-Otin C., Smith B., Atkinson S.J., Stanton H., Hembry R.M., Murphy G. Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme. J. Biol. Chem. 1996, 271:17124-17131.
28. Kolf C.M., Cho E., Tuan R.S. Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res. Ther. 2007, 9:204.
29. Lauer-Fields J.L., Fields G.B. Triple-helical peptide analysis of collagenolytic protease activity. Biol. Chem. 2002, 383:1095-1105.
30. Lauer-Fields J.L., Broder T., Sritharan T., Chung L., Nagase H., Fields G.B. Kinetic analysis of matrix metalloproteinase activity using fluorogenic triple-helical substrates. Biochemistry 2001, 40:5795-5803.
31. Lee O.K., Kuo T.K., Chen W.M., Lee K.D., Hsieh S.L., Chen T.H. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004, 103:1669-1675.
32. Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 2007, 17:107-117.
33. Lombard C., Saulnier J., Wallach J. Assays of matrix metalloproteinases (MMPs) activities: a review. Biochimie 2005, 87:265-272.
34. Lozito T.P., Tuan R.S. Mesenchymal stem cells inhibit both endogenous and exogenous MMPs via secreted TIMPs. J. Cell. Physiol. 2011, 226:385-396.
35. Matrisian L.M., Sledge G.W., Mohla S. Extracellular proteolysis and cancer: meeting summary and future directions. Cancer Res. 2003, 63:6105-6109.
36. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
37. Nesti L.J., Jackson W.M., Shanti R.M., Koehler S.M., Aragon A.B., Bailey J.R., Sracic M.K., Freedman B.A., Giuliani J.R., Tuan R.S. Differentiation potential of multipotent progenitor cells derived from war-traumatized muscle tissue. J. Bone Joint Surg. Am. 2008, 90:2390-2398.
38. Noth U., Osyczka A.M., Tuli R., Hickok N.J., Danielson K.G., Tuan R.S. Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J. Orthop. Res. 2002, 20:1060-1069.
39. Perry B.C., Zhou D., Wu X., Yang F.C., Byers M.A., Chu T.M., Hockema J.J., Woods E.J., Goebel W.S. Collection, cryopreservation, and characterization of human dental pulp-derived mesenchymal stem cells for banking and clinical use. Tissue Eng. Part C Methods 2008, 14:149-156.
40. Petrie C., Tholpady S., Ogle R., Botchwey E. Proliferative capacity and osteogenic potential of novel dura mater stem cells on poly-lactic-co-glycolic acid. J. Biomed. Mater. Res. A 2008, 85:61-71.
41. Ray J.M., Stetler-Stevenson W.G. The role of matrix metalloproteases and their inhibitors in tumour invasion, metastasis and angiogenesis. Eur. Respir. J. 1994, 7:2062-2072.
42. Ries C., Egea V., Karow M., Kolb H., Jochum M., Neth P. MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines. Blood 2007, 109:4055-4063.
43. Rzhaninova A.A., Gornostaeva S.N., Goldshtein D.V. Isolation and phenotypical characterization of mesenchymal stem cells from human fetal thymus. Bull. Exp. Biol. Med. 2005, 139:134-140.
44. Sarugaser R., Lickorish D., Baksh D., Hosseini M.M., Davies J.E. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 2005, 23:220-229.
45. Sekiya I., Larson B.L., Vuoristo J.T., Cui J.G., Prockop D.J. Adipogenic differentiation of human adult stem cells from bone marrow stroma (MSCs). J. Bone Miner. Res. 2004, 19:256-264.
46. Shi S., Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J. Bone Miner. Res. 2003, 18:696-704.
47. Shih D.T., Lee D.C., Chen S.C., Tsai R.Y., Huang C.T., Tsai C.C., Shen E.Y., Chiu W.T. Isolation and characterization of neurogenic mesenchymal stem cells in human scalp tissue. Stem Cells 2005, 23:1012-1020.
48. Stetler-Stevenson W.G. Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J. Clin. Invest. 1999, 103:1237-1241.
49. Traktuev D.O., Merfeld-Clauss S., Li J., Kolonin M., Arap W., Pasqualini R., Johnstone B.H., March K.L. 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.
50. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 2003, 92:827-839.
51. Worley J.R., Thompkins P.B., Lee M.H., Hutton M., Soloway P., Edwards D.R., Murphy G., Knauper V. Sequence motifs of tissue inhibitor of metalloproteinases 2 (TIMP-2) determining progelatinase A (proMMP-2) binding and activation by membrane-type metalloproteinase 1 (MT1-MMP). Biochem. J. 2003, 372:799-809.
52. Yen B.L., Huang H.I., Chien C.C., Jui H.Y., Ko B.S., Yao M., Shun C.T., Yen M.L., Lee M.C., Chen Y.C. Isolation of multipotent cells from human term placenta. Stem Cells 2005, 23:3-9.
53. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001, 7:211-228.