Matrix remodeling as stem cell recruitment event: A novel in vitro model for homing of human bone marrow stromal cells to the site of injury shows crucial role of extracellular collagen matrix

Matrix Biology

Volumn 29, Issue 8, 2010, Pages 657-663

  Mauney, Joshua ^b   Olsen, Bjorn R ^a   Volloch, Vladimir ^a  

^a HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Extracellular collagen matrix; Homing of mesenchymal stem cells; Matrix remodeling as stem cell recruitment

Indexed keywords

AMINOETHYLBENZENSULFONYL FLUORIDE; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; HIGH TEMPERATURE REQUIREMENT PROTEIN A1; LEUPEPTIN; MARIMASTAT; PROTEINASE; PROTEINASE INHIBITOR; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ARTICLE; BONE MARROW CELL; BONE TISSUE; CELL HOMING; CELL MEMBRANE; CELL MIGRATION; CELL SECRETION; CELL STRESS; CELLULAR DISTRIBUTION; CHEMOTAXIS; CONTROLLED STUDY; EXTRACELLULAR COLLAGEN MATRIX; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; MUSCLE TISSUE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SECRETION; SIMULATION; STROMA CELL; TEMPERATURE STRESS; TISSUE CULTURE;

ADULT STEM CELLS; ANTIBODIES; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN; COLLAGEN TYPE I; COLLAGEN TYPE IV; CULTURE MEDIA, CONDITIONED; CYSTEINE PROTEINASE INHIBITORS; EXTRACELLULAR MATRIX; FIBROBLASTS; HEAT-SHOCK RESPONSE; HUMANS; IMMUNOPRECIPITATION; MESENCHYMAL STEM CELLS; REGENERATION; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; STROMAL CELLS; WOUNDS AND INJURIES;

EID: 78649446275     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2010.08.008     Document Type: Article

References (60)

1. Albini A., Adelmann-Grill B. Collagenolytic cleavage products of collagen type I as chemoattractants for human dermal fibroblasts. Eur. J. Cell Biol. 1985, 36:104-107.
2. Baldi A., De Luca A., Felsani A., Baldi F., Catricalà C., Amantea A., Noonan D.M., Albini A., Natali P.G., Lombardi D., Paggi M.G. The HtrA1 serine protease is down-regulated during human melanoma progression and represses growth of metastatic melanoma cells. Oncogene 2002, 21:6684-6688.
3. Bantubungi K., Blum D., Cuvelier L., Wislet-Gendebien S., Rogister B., Brouillet E., Schiffmann S. Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of Huntington's disease. Mol. Cell. Neurosci. 2008, 37:454-470.
4. Baron R. Molecular mechanisms of bone resorption by the osteoclast. Anat. Rec. 1989, 224(2):317-324.
5. Baron R., Neff L., Louvard D., Courtoy P.J. Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J. Cell Biol. 1985, 101:2210-2222.
6. Belema-Bedada F., Uchida S., Martire A., Kostin S., Braun T. Efficient homing of multipotent adult MSCs depends on FROUNT-mediated clustering of CCR2. Cell Stem Cell 2008, 2:566-575.
7. Bianco P., Robey P., Simmons P. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2008, 2:313-319.
8. Bowers R.R., Kim J.W., Otto T.C., Lane M.D. Stable stem cell commitment to the adipocyte lineage by inhibition of DNA methylation: role of the BMP-4 gene. Proc. Natl Acad. Sci. USA 2006, 103:13022-13027.
9. Canfield A.E., Hadfield K.D., Rock C.F., Wylie E.C., Wilkinson F.L. HtrA1: a novel regulator of physiological and pathological matrix mineralization?. Biochem. Soc. Trans. 2007, 35(Pt 4):669-671.
10. Chiang T., Postlethwaite A., Beachey E., Seyer J., Kang A. Binding of cemotactic collagen-derived peptides to fibriblasts, the relationship to fibroblast chemotaxis. J. Clin. Invest. 1978, 62:916-922.
11. Clausen T., Southan C., Ehrmann M. The HtrA family of proteases: implications for protein composition and cell fate. Mol. Cell 2002, 10:443-455.
12. da Silva Meirelles L., Chagastelles P., Nardi N. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 2006, 119:2204-2213.
13. da Silva Meirelles L., Caplan A., Nardi N. In search of the invivo identity of mesenchymal stem cells. Stem Cells 2008, 26:2287-2299.
14. De Becker P., Van Hummelen M., Bakkus I., Vande Broek J., De Wever M., De Waele, 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.
15. De Luca A., De Falco M., Fedele V., Cobellis L., Mastrogiacomo A., Laforgia V., Tuduce I.L., Campioni M., Giraldi D., Paggi M.G., Baldi A. The serine protease HtrA1 is upregulated in the human placenta during pregnancy. J. Histochem. Cytochem. 2004, 52:885-892.
16. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Prockop A., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
17. Fuchs E., Tumbar T., Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004, 116:769-778.
18. Gotoh Y., Fujisawa K., Satomura K., Nagayama M. Osteogenesis by human osteoblastic cells in diffusion chamber in vivo. Calcif. Tissue Int. 1995, 56:246-251.
19. Grau S., Baldi A., Bussani R., Tian X., Stefanescu R., Przybylski M., Richards P., Jones S.A., Shridhar V., Clausen T., Ehrmann M. Implications of the serine protease HtrA1 in amyloid precursor protein processing. Proc. Natl Acad. Sci. USA 2005, 102:6021-6026.
20. Grau S., Richards P.J., Kerr B., Hughes C., Caterson B., Williams A.S., Junker U., Jones S.A., Clausen T., Ehrmann M. The role of human HtrA1 in arthritic disease. J. Biol. Chem. 2006, 281:6124-6129.
21. Hadfield K.D., Rock C.F., Inkson C.A., Dallas S.L., Sudre L., Wallis G.A., Boot-Handford R.P., Canfield A.E. HtrA1 inhibits mineral deposition by osteoblasts: requirement for the protease and PDZ domains. J. Biol. Chem. 2008, 283:5928-5938.
22. He Q., Wan C., Li G. Concise review: multipotent mesenchymal stromal cells in blood. Stem Cells 2007, 25:69-77.
23. Hordijk P. Endothelial signaling in leukocyte transmigration. Cell Biochem. Biophys. 2003, 38:305-312.
24. Hu S.I., Carozza M., Klein M., Nantermet P., Luk D., Crowl R.M. Human HtrA, an evolutionarily conserved serine protease identified as a differentially expressed gene product in osteoarthritic cartilage. J. Biol. Chem. 1998, 273:34406-34412.
25. Jilka R.L., Weinstein R.S., Takahashi K., Parfitt A.M., Manolagas S.C. Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J. Clin. Invest. 1996, 97:1732-1738.
26. Kuznetsov S., Mankani M.H., Gronthos S., Satomura K., Bianco P., Robey P.G. Circulating skeletal stem cells. J. Cell Biol. 2001, 153:1133-1140.
27. Laskin D., Kimura T., Sakakibara S., Riley D., Berg R. Chemotactic activity of collagen-like polypeptides for human peripheral blood neutrophils. J. Leukoc. Biol. 1986, 39:255-266.
28. Launay S., Maubert E., Lebeurrier N., Tennstaedt A., Campioni M., Docagne F., Gabriel C., Dauphinot L., Potier M.C., Ehrmann M., Baldi A., Vivien D. HtrA1-dependent proteolysis of TGF-beta controls both neuronal maturation and developmental survival. Cell Death Differ. 2008, 15:1408-1416.
29. Lee R., Kim B., Choi I., Kim H., Choi H., Suh K., Bae Y., Jung J. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell. Phys. and Biochem. 2004, 14:311-324.
30. Lee P., Kim J.W., Bang O.Y., Ahn Y.H., Joo I.S., Huh K. Autologous mesenchymal stem cell therapy delays the progression of neurological deficits in patients with multiple system atrophy. Clin. Pharmacol. Ther. 2008, 83:723-730.
31. Malone J., Richards M., Jeffrey J. Recruitment of peripheral mononuclear cells by mammalian collagenase digest of type I collagen. Matrix 1991, 11:289-295.
32. Mauney J., Volloch V. Progression of human bone marrow stromal cells into both osteogenic and adipogenic lineages is differentially regulated by structural conformation of collagen I matrix via distinct signaling pathways. Matrix Biol. 2009, 10.1016/j.matbio.04.003.
33. Mauney J., Volloch V. Collagen I matrix contributes to determination of adult human stem cells lineage via differential, structural conformation-specific elicitation of cellular stress response. Matrix Biol. 2009, 10.1016/j.matbio.04.002.
34. Mauney, J. and Volloch, V. 2009c. Extracellular collagen IV matrix in denatured structural conformation drives highly efficient stress-resistant adipogenesis of bone marrow stromal cells: implications for obesity. doi:10.1016/j.matbio.2009.09.002.
35. Mauney J.R., Kaplan D.L., Volloch V. Matrix-mediated retention of osteogenic differentiation potential by human adult bone marrow stromal cells during ex vivo expansion. Biomaterials 2004, 25:3233-3243.
36. Mauney J.R., Volloch V., Kaplan D.L. Matrix-mediated retention of adipogenic differentiation potential by human adult bone marrow-derived mesenchymal stem cells during ex vivo expansion. Biomaterials 2005, 26:6167-6175.
37. Mauney J.R., Kirker-Head C., Abrahamson L., Gronowicz G., Volloch V., Kaplan D.L. Matrix-mediated retention of in vitro osteogenic differentiation potential and in vivo bone-forming capacity by human adult bone marrow-derived mesenchymal stem cells during ex vivo expansion. J. Biomed. Mater. Res. 2006, 79:464-475.
38. Mauney J., Nguyen T., Gillen K., Kirker-Head C., Gimble J., Kaplan D. Engineering adipose-like tissue in vitro and in vivo utilizing human bone marrow and adipose-derived mesenchymal stem cells with silk fibroin 3D scaffolds. Biomaterials 2007, 28:5280-5290.
39. Oka C., Tsujimoto R., Kajikawa M., Koshiba-Takeuchi K., Ina J., Yano M., Tsuchiya A., Ueta Y., Soma A., Kanda H., Matsumoto M., Kawaichi M. HtrA1 serine protease inhibits signaling mediated by Tgfbeta family proteins. Development 2004, 131:1041-1053.
40. Petite H., Viateau V., Bensaid W., Meunier A., de Pollak C., Bourguignon M., Oudina K., Sedel L., Guillemin G. Tissue-engineered bone regeneration. Nat. Biotechnol. 2000, 18:959-963.
41. Phinney D., Prockop D.J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair current views. Stem Cells 2007, 25:2896-2902.
42. Ponte A., Marais E., Gallay N., Langonne A., Delorme B., Herault O., Charbord P., Domenech J. The invitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells 2007, 25:1737-1745.
43. Postlethwaite A., Seyer J., Kang A. Chemotactic attraction of human fibroblasts to type I, II, and III collagens and collagen-derived peptides. Proc. Natl Acad. Sci. USA 1978, 75:871-875.
44. 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.
45. Rochefort G., Delorme A.Lopez, Herault O., Bonnet P., Charbord P., Eder V., Domenech J. Multipotential mesenchymal stem cells are mobilized into peripheral blood by hypoxia. Stem Cells 2006, 24:2202-2208.
46. Sackstein R., Merzaban J.S., Cain D.W., Dagia N.M., Spencer J.A., Lin C.P., Wohlgemuth R. Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat. Med. 2008, 14:181-187.
47. Scheven B., Hamilton N., Farquharson C., Rucklidge G., Robins S. Immunohistochemical localization of native and denatured collagen types I and II in fetal and adult rat bones. Bone 1988, 9:407-414.
48. Steingen C., Brenig F., Baumgartner L., Schmidt J., Bloch W. Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J. Mol. Cell. Card. 2008, 44:1072-1084.
49. Tocharus J., Tsuchia A., Kajikawa M., Ueta Y., Oka C., Kawaichi M. Developmentally regulated expression of mouse HTRA3 and its role as an inhibitor of TGF-beta signaling. Dev. Growth Differ. 2004, 46:257-274.
50. Tondreau T., Meuleman N., Delforge A., Dejeneffe M., Leroy R., Massy M., Mortier C., Bron D., Lagneaux L. Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells 2005, 23:1105-1112.
51. Tsuchiya A., Yano M., Tocharus J., Kojima H., Fukumoto M., Kawaichi M., Oka C. Expression of mouse HtrA1 serine protease in normal bone and cartilage and its upregulation in joint cartilage damaged by experimental arthritis. Bone 2005, 37:323-336.
52. Turner C.H., Owan I., Alvey T., Hulman J., Hock J.M. Recruitment and proliferative responses of osteoblasts after mechanical loading in vivo determined using sustained-release bromodeoxyuridine. Bone 1998, 22:463-469.
53. Vaes G. Cellular biology and biochemical mechanism of bone resorption. A review of the formation, activation, and mode of action of osteoclasts. Clin Orthop Relat Res 1988, 231:239-271.
54. Volloch V., Kaplan D. Matrix-mediated cellular rejuvenation. Matrix Biol. 2002, 21:533-543.
55. Wang C.-H., Cherng W.-J., Yang N.-I., Kuo L.-T., Hsu C.-M., Yeh H.-I., Lan Y.-J., Yeh C.-H., Stanford W.L. Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler. Thromb. Vasc. Biol. 2008, 28:54-60.
56. Wang J., He A., Hu X., Jiang Y., Sun Y., Jiang J., Gui C., Wang Y., Chen H. Anoxic preconditioning: a way to enhance the cardioprotection of mesenchymal stem cells. Int. J. Cardiol. 2008, 10.1016/j.ijcard.2007.11.096.
57. Wexler S.A., Donaldson C., Denning-Kendall P., Rice C., Bradley B., Hows J.M. Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. Br. J. Haematol. 2003, 121:368-374.
58. Yang Z., Camp N.J., Sun H., Tong Z., Gibbs D., Cameron D.J., Zhao Y., Pearson E., Li X., Chien J., Dewan A., Harmon J., Bernstein P.S., Shridhar V., Zabriskie N.A., Hoh J., Howes K., Zhang K. A variant of the HTRA1 gene increases susceptibility to age-related macular degeneration. Science 2006, 314:992-993.
59. 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.
60. Zurawa-Janicka D., Kobiela J., Stefaniak T., Wozniak A., Narkiewicz J., Wozniak M., Limon J., Lipinska B. Changes in expression of serine proteases HtrA1 and HtrA2 during estrogen-induced oxidative stress and nephrocarcinogenesis in male Syrian hamster. Acta Biochim. Pol. 2008, 55:9-19.