Differential effects of bone morphogenetic protein-2 and transforming growth factor-β1 on gene expression of collagen-modifying enzymes in human adipose tissue-derived mesenchymal stem cells

Tissue Engineering - Part A

Volumn 15, Issue 8, 2009, Pages 2213-2225

  Knippenberg, Marlene ^a,b   Helder, Marco N ^b   Doulabi, Behrouz Zandieh ^b   Bank, Ruud A ^a,c   Wuisman, Paul I J M ^b   Klein Nulend, Jenneke ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c TNO   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACTIVITY; BIOMECHANICS; BONE; CATALYSTS; CELL CULTURE; CELLS; COLLAGEN; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYMES; FLOWCHARTING; GENE EXPRESSION; MECHANICAL PROPERTIES; PEPTIDES;

ADIPOSE TISSUE; ALKALINE PHOSPHATASE ACTIVITY; BONE MORPHOGENETIC PROTEIN-2; BONE TISSUE; BONE TISSUE ENGINEERING; DIFFERENTIAL EFFECT; EXTRACELLULAR MATRICES; GROWTH FACTOR; HUMAN ADIPOSE TISSUE; HYDROXYLASES; LYSYL OXIDASE; MESENCHYMAL STEM CELL; OSTEOGENIC DIFFERENTIATION; PHYSICAL AND MECHANICAL PROPERTIES; POST-TRANSLATIONAL MODIFICATIONS; PROCOLLAGEN; TRANSFORMING GROWTH FACTORS; TYPE I COLLAGEN;

TISSUE ENGINEERING;

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 1; LYSYL HYDROXYLASE 1; LYSYL HYDROXYLASE 2; LYSYL HYDROXYLASE 3; PROCOLLAGEN ALPHA2(I); PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; PROTEIN LYSINE 6 OXIDASE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ADIPOSE TISSUE DERIVED MESENCHYMAL STEM CELL; ARTICLE; BONE MATRIX; CONTROLLED STUDY; ENZYME BINDING; EXTRACELLULAR MATRIX; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCHYMAL STEM CELL; PHYSICAL CHEMISTRY; PLOD1 GENE; PLOD2 GENE; PLOD3 GENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TISSUE ENGINEERING;

ADIPOSE TISSUE; ADOLESCENT; ADULT; ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN; CORE BINDING FACTOR ALPHA 1 SUBUNIT; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MESENCHYMAL STEM CELLS; OSTEOPONTIN; PROCOLLAGEN-LYSINE, 2-OXOGLUTARATE 5-DIOXYGENASE; PROTEIN-LYSINE 6-OXIDASE; TRANSFORMING GROWTH FACTOR BETA1;

EID: 68749116411     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2007.0184     Document Type: Article

References (62)

1. Reddi, A.H. Role of morphogenetic proteins in skeletal tissue engineering and regeneration. Nat Biotechnol 16, 247, 1998.
2. Cowan, C.M., Shi, Y.Y., Aalami, O.O., Chou, Y.F., Mari, C., Thomas, R., Quarto, N., Contag, C.H., Wu, B., and Longaker, M.T. Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22, 560, 2004.
3. Helder, M.N., Knippenberg, M., Klein-Nulend, J., and Wuisman, P.I. Stem cells from adipose tissue allow challenging new concepts for regenerative medicine. Tissue Eng 13, 1799, 2007.
4. Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz, A.J., Benhaim, P., Lorenz, H.P., and Hedrick, M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7, 211, 2001.
5. Zuk, P.A., Zhu, M., Ashjian, P., de Ugarte, D.A., Huang, J.I., Mizuno, H., Alfonso, Z.C., Fraser, J.K., Benhaim, P., and Hedrick, M.H. Human adipose tissue is a source of multi-potent stem cells. Mol Biol Cell 13, 4279, 2002.
6. Knippenberg, M., Helder, M.N., Zandieh, Doulabi, B., Se-meins, C.M., Wuisman, P.I., and Klein-Nulend, J. Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng 11, 1780, 2005.
7. Knippenberg, M., Helder, M.N., Blieck-Hogervorst, J.M., Wuisman, P.I., and Klein-Nulend, J. Prostaglandins differentially affect osteogenic differentiation of human adipose tissue-derived mesenchymal stem cells. Tissue Eng 13, 2495, 2007.
8. Knippenberg, M., Helder, M.N., Zandieh Doulabi, B., Wuisman, P.I., and Klein-Nulend, J. Osteogenesis versus chondrogenesis by BMP-2 and BMP-7 in adipose stem cells. Biochem Biophys Res Commun 342, 902, 2006.
9. Samartzis, D., Khanna, N., Shen, F.H., and An, H.S. Update on bone morphogenetic proteins and their application in spine surgery. J Am Coll Surg 200, 236, 2005.
10. Burkus, J.K. Surgical treatment of the painful motion segment: matching technology with indications. Spine 30, S7, 2005.
11. Katz, J.L. Hard tissue as a composite material. I. Bounds on the elastic behavior. J Biomech 4, 455, 1971.
12. Gelse, K., Poschl, E., and Aigner, T. Collagens - structure, function, and biosynthesis. Adv Drug Delivery Rev 55, 1531, 2003.
13. Yeowell, H.N., and Walker, L.C Mutations in the lysyl hydroxylase 1 gene that result in enzyme deficiency and the clinical phenotype of Ehlers-Danlos syndrome type VI. Mol Genet Metab 71, 212, 2000.
14. Hautala, T., Byers, M.G., Eddy, R.L., Shows, T.B., Kivirikko, K.I., and Myllyla, R. Cloning of human lysyl hydroxylase: complete cDNA-derived amino acid sequence and assignment of the gene (PLOD) to chromosome Ip36.3-p36.2. Genomics 13, 62, 1992.
15. Valtavaara, M., Papponen, H., Pirttila, A.M., Hiltunen, K., Helander, H., and Myllyla, R. Cloning and characterization of a novel human lysyl hydroxylase isoform highly expressed in pancreas and muscle. J Biol Chem 272, 6831, 1997.
16. Valtavaara, M., Szpirer, C., Szpirer, J., and Myllyla, R. Primary structure, tissue distribution, and chromosomal localization of a novel isoform of lysyl hydroxylase (lysyl hydroxylase 3). J Biol Chem 273, 12881, 1998.
17. Rautavuoma, K., Takaluoma, K., Passoja, K., Pirskanen, A., Kvist, A.P., Kivirikko, K.I., and Myllyharju, J. Characterization of three fragments that constitute the monomers of the human lysyl hydroxylase isoenzymes 1-3. The 30-kDa N-terminal fragment is not required for lysyl hydroxylase activity. J Biol Chem 277, 23084, 2002.
18. Steinmann, B., Eyre, D.R., and Shao, P. Urinary pyridinoline cross-links in Ehlers-Danlos syndrome type VI. Am J Hum Genet 57, 1505, 1995.
19. Ruotsalainen, H., Vanhatupa, S., Tampio, M., Sipila, L., Valtavaara, M., and Myllyla, R. Complete genomic structure of mouse lysyl hydroxylase 2 and lysyl hydroxylase 3/col-collagen glucosyltransferase. Matrix Biol 20, 137, 2001.
20. Wang, C., Luosujarvi, H., Heikkinen, J., Risteli, M., Uitto, L., and Myllyla, R. The third activity for lysyl hydroxylase 3: galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol 21, 559, 2002.
21. van der Slot, A.J., Zuurmond, A.M., Bardoel, A.F., Wijmenga, C., Pruijs, H.E., Sillence, D.O., Brinckmann, J., Abraham, D.J., Black, C.M., Verzijl, N., Degroot, J., Hane-maaijer, R., TeKoppele, J.M., Huizinga, T.W., and Bank, R.A. Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem 278, 40967, 2003.
22. Passoja, K., Rautavuoma, K., Ala-Kokko, L., Kosonen, T., and Kivirikko, K.I. Cloning and characterization of a third human lysyl hydroxylase isoform. Proc Natl Acad Sci USA 95, 10482, 1998.
23. Bank, R. A., Robins, S.P., Wijmenga, C., Breslau-Siderius, L.J., Bardoel, A.F., van der Sluijs, H.A., Pruijs, H.E., and TeKoppele, J.M. Defective collagen crosslinking in bone, but not in ligament or cartilage, in Bruck syndrome: indications for a bone-specific telopeptide lysyl hydroxylase on chromosome 17. Proc Natl Acad Sci USA 96, 1054, 1999.
24. Ha-Vinh, R., Alanay, Y., Bank, R.A., Campos-Xavier, A.B., Zankl, A., Superti-Furga, A., and Bonafe, L. Phenotypic and molecular characterization of Bruck syndrome (osteogenesis imperfecta with contractures of the large joints) caused by a recessive mutation in PLOD2. Am J Med Genet A 131, 115, 2004.
25. Brenner, R.E., Vetter, U., Stoss, H., Muller, P.K., and Teller, W.M. Defective collagen fibril formation and mineralization in osteogenesis imperfecta with congenital joint contractures (Bruck syndrome). Eur J Pediatr 152, 505, 1993.
26. Dragoo, J.L., Choi, J.Y., Lieberman, J.R., Huang, J., Zuk, P.A., Zhang, J., Hedrick, M.H., and Benhaim, P. Bone induction by BMP-2 transduced stem cells derived from human fat. J Orthop Res 21, 622, 2003.
27. Lieb, E., Milz, S., Vogel, T., Hacker, M., Dauner, M., and Schulz, M.B. Effects of transforming growth factor betal on bonelike tissue formation in three-dimensional cell culture. I. Culture conditions and tissue formation. Tissue Eng 10, 1399, 2004.
28. Carlisle, E., and Fischgrund, J.S. Bone morphogenetic proteins for spinal fusion. Spine J 5, 240S, 2005.
29. Kanaan, R.A., and Kanaan, L.A. Transforming growth factor betal, bone connection. Med Sci Monit 12, RA164, 2006.
30. Tsumaki, N., and Yoshikawa, H. The role of bone morphogenetic proteins in endochondral bone formation. Cytokine Growth Factor Rev 16, 279, 2005.
31. Wozney, J.M., Rosen, V., Celeste, A.J., Mitsock, L.M., Whitters, M.J., Kriz, R.W., Hewick, R.M., and Wang, E.A. Novel regulators of bone formation: molecular clones and activities. Science 242, 1528, 1988.
32. Ozkaynak, E., Rueger, D.C., Drier, E.A., Corbett, C., Ridge, R.J., Sampath, T.K., and Oppermann, H. OP-1 cDNA encodes an osteogenic protein in the TGF-beta family. EMBO J 9, 2085, 1990.
33. Bonewald, L.F. Transforming growth factor-beta. In: Bilezikian, J.P., Raisz, L.G., and Rodan, G.A., eds. Principles of Bone Biology. San Diego, CA: Academic Press, 2002, pp. 903-918.
34. Lieb, E., Vogel, T., Milz, S., Dauner, M., and Schulz, M.B. Effects of transforming growth factor betal on bonelike tissue formation in three-dimensional cell culture. II: Osteo blastic differentiation. Tissue Eng 10, 1414, 2004.
35. Kaku, M., Mochida, Y., Atsawasuwan, P., Parisuthiman, D., and Yamauchi, M. Post-translational modifications of collagen upon BMP-induced osteoblast differentiation. Biochem Biophys Res Commun 359, 463, 2007.
36. Lu, Z.F., Zandieh, D.B., Wuisman, P.I., Bank, R.A., and Helder, M.N. Differentiation of adipose stem cells by nucleus pulposus cells: configuration effect. Biochem Biophys Res Commun 359, 991, 2007.
37. Lefebvre, V., Behringer, R.R., and de Cormbrugghe, B. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthritis Cartilage 9 Suppl A, S69, 2001.
38. Oedayrajsingh-Varma, M.J., van Ham, S.M., Knippenberg, M., Helder, M.N., Klein-Nulend, J., Schouten, T.E., Ritt, M.J., and van Milligen, F.J. Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 8, 166, 2006.
39. Tjabringa, G.S., Vezeridis, P.S., Zandieh-Doulabi, B., Helder, M.N., Wuisman, P.I., and Klein-Nulend, J. Polyamines modulate nitric oxide production and COX-2 gene expression in response to mechanical loading in human adipose tissue-derived mesenchymal stem cells. Stem Cells 24, 2262, 2006.
40. Gronthos, S., Franklin, D.M., Leddy, H.A., Robey, P.G., Storms, R.W., and Gimble, J.M. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189, 54, 2001.
41. Lowry, O.H. Micromethods for the assay of enzyme. II Specific procedure. Alkaline phosphatase. Methods Enzymol 4, 371, 1955.
42. van der Slot, A.J., Zuurmond, A.M., van den Bogaerdt, A.J., Ulrich, M.M., Middelkoop, E., Boers, W., Karel, R.H., Degroot, J., Huizinga, T.W., and Bank, R.A. Increased formation of pyridinoline cross-links due to higher telopeptide lysyl hydroxylase levels is a general fibrotic phenomenon. Matrix Biol 23, 251, 2004.
43. Bank, R.A., Jansen, E.J., Beekman, B., and te Koppele, J.M. Amino acid analysis by reverse-phase high-performance liquid chromatography: improved derivatization and detection conditions with 9-fluorenylmethyl chloroformate. Anal Biochem 240, 167, 1996.
44. Bank, R.A., Beekman, B., Verzijl, N., de Roos, J.A., Sakkee, A.N., and TeKoppele, J.M. Sensitive fluorimetric quantitation of pyridinium and pentosidine crosslinks in biological samples in a single high-performance liquid chromato-graphic run. J Chromatogr B Biomed Sci Appl 703, 37, 1997.
45. Robins, S.P., Duncan, A., Wilson, N., and Evans, B.J. Standardization of pyridinium crosslinks, pyridinoline and deoxypyridinoline, for use as biochemical markers of collagen degradation. Clin Chem 42, 1621, 1996.
46. Reddi, A.H. Morphogenesis and tissue engineering of bone and cartilage: inductive signals, stem cells, and biomimetic biomaterials. Tissue Eng 6, 351, 2000.
47. Viguet-Carrin, S., Garnero, P., and Delmas, P.D. The role of collagen in bone strength. Osteoporos Int 17, 319, 2006.
48. Uzawa, K., Grzesik, W.J., Nishiura, T., Kuznetsov, S.A., Robey, P.G., Brenner, D.A., and Yamauchi, M. Differential expression of human lysyl hydroxylase genes, lysine hy-droxylation, and cross-linking of type I collagen during os-teoblastic differentiation in vitro. J Bone Miner Res 14, 1272, 1999.
49. Wang, C., Valtavaara, M., and Myllyla, R. Lack of collagen type specificity for lysyl hydroxylase isoforms. DNA Cell Biol 19, 71, 2000.
50. Pornprasertsuk, S., Duarte, W.R., Mochida, Y., and Yamauchi, M. Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J Bone Miner Res 19, 1349, 2004.
51. Pornprasertsuk, S., Duarte, W.R., Mochida, Y., and Yamauchi, M. Overexpression of lysyl hydroxylase-2b leads to defective collagen fibrillogenesis and matrix mineralization. J Bone Miner Res 20, 81, 2005.
52. Mercer, D.K., Nicol, P.F., Kimbembe, C., and Robins, S.P. Identification, expression, and tissue distribution of the three rat lysyl hydroxylase isoforms. Biochem Biophys Res Commun 307, 803, 2003.
53. Walker, L.C., Overstreet, M.A., Siddiqui, A., de Paepe, A., Ceylaner, G., Malfait, F., Symoens, S., Atsawasuwan, P., Yamauchi, M., Ceylaner, S., Bank, R.A., and Yeowell, H.N. A novel mutation in the lysyl hydroxylase 1 gene causes decreased lysyl hydroxylase activity in an Ehlers-Danlos VIA patient. J Invest Dermatol 124, 914, 2005.
54. Salo, A.M., Wang, C., Sipila, L., Sormunen, R., Vapola, M., Kervinen, P., Ruotsalainen, H., Heikkinen, J., and Myllyla, R. Lysyl hydroxylase 3 (LH3) modifies proteins in the extracellular space, a novel mechanism for matrix remodeling. J Cell Physiol 207, 644, 2006.
55. Takashi, M., Tsubaki, S., Tsuzuki, T., Duarte, W.R., Yamauchi, M., and Sato, H. Differential gene expression of collagen-binding small leucine-rich proteoglycans and lysyl hydroxylases, during mineralization by MC3T3-E1 cells cultured on titanium implant material. Eur J Oral Sci 113, 225, 2005.
56. Hong, H.H., Pischon, N., Santana, R.B., Palamakumbura, A.H., Chase, H.B., Gantz, D., Guo, Y., Uzel, M.I., Ma, D., and Trackman, P.C. A role for lysyl oxidase regulation in the control of normal collagen deposition in differentiating os-teoblast cultures. J Cell Physiol 200, 53, 2004.
57. Trackman, P.C. Diverse biological functions of extracellular collagen processing enzymes. J Cell Biochem 96, 927, 2005.
58. Lucero, H.A., and Kagan, H.M. Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell Mol Life Sci 63, 2304, 2006.
59. Gerstenfeld, L.C., Riva, A., Hodgens, K., Eyre, D.R., and Landis, W.J. Post-translational control of collagen fi-brillogenesis in mineralizing cultures of chick osteoblasts. J Bone Miner Res 8, 1031, 1993.
60. Feres-Filho, E.J., Choi, Y.J., Han, X., Takala, T.E., and Trackman, P.C. Pre- and post-translational regulation of lysyl oxidase by transforming growth factor-beta 1 in osteo-blastic MC3T3-E1 cells. J Biol Chem 270, 30797, 1995.
61. Hong, H.H., Uzel, M.I., Duan, C., Sheff, M.C., and Trackman, P.C. Regulation of lysyl oxidase, collagen, and connective tissue growth factor by TGF-betal and detection in human gingiva. Lab Invest 79, 1655, 1999.
62. Wassen, M.H., Lammens, J., TeKoppele, J.M., Sakkers, R.J., Liu, Z., Verbout, A.J., and Bank, R.A. Collagen structure regulates fibril mineralization in osteogenesis as revealed by cross-link patterns in calcifying callus. J Bone Miner Res 15, 1776, 2000.