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 Biology

Volumn 28, Issue 5, 2009, Pages 239-250

  Mauney, Josh ^a   Volloch, Vladimir ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Adult human stem cells; Matrix mediated differentiation; Structural conformation of extracellular matrix

Indexed keywords

COLLAGEN TYPE 1; HEAT SHOCK PROTEIN 90; MITOGEN ACTIVATED PROTEIN KINASE P38;

ADIPOCYTE; ADIPOGENESIS; ADULT; AGING; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; BONE REMODELING; CELL DIFFERENTIATION; CELL LINEAGE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MUSCULOSKELETAL SYSTEM; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ADIPOGENESIS; ADULT; ANIMALS; BIOLOGICAL MARKERS; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; COLLAGEN TYPE I; EXTRACELLULAR MATRIX; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; OSTEOGENESIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN CONFORMATION; PROTEIN DENATURATION; SIGNAL TRANSDUCTION; STROMAL CELLS;

EID: 67649342034     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2009.04.003     Document Type: Article

References (74)

1. Abraham D., Podar K., Pacher M., Kubicek M., Welzel N., Hemmings B.A., Dilworth S.M., Mischak H., Kolch W., and Baccarini M. Raf-1-associated protein phosphatase 2A as a positive regulator of kinase activation. J. Biol. Chem. 275 (2000) 22300-22304
2. Altman G.H., Horan R.L., Martin I., and Farhadi J. Cell differentiation by mechanical stress. FASEB J. 16 (2002) 270-272
3. Baron R. Molecular mechanisms of bone resorption by the osteoclast. Anat. Rec. 224 2 (1989) 317-324 (Review)
4. Baron R., Neff L., Louvard D., and 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. 101 6 (1985) 2210-2222
5. Birkedal-Hansen H. Role of matrix metalloproteinases in human periodontal diseases. J. Periodontol. 64 (1993) 474-484
6. Blanco-Aparicio C., Torres J., and Pulido R. A novel regulatory mechanism of MAP kinases activation and nuclear translocation mediated by PKA and the PTP-SL tyrosine phosphatase. J. Cell Biol. 147 (1999) 1129-1136
7. Chavey C., Mari B., Monthouel M.N., Bonnafous S., Anglard P., Van Obberghen E., and Tartare-Deckert S. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J. Biol. Chem. 278 (2003) 11888-11896
8. Chetoui N., Gendron S., Chamoux E., and Aoudjit F. Collagen type I-mediated activation of ERK/MAP kinase is dependent on Ras, Raf-1 and protein phosphatase 2A in Jurkat T cells. Mol. Immunol. 43 (2006) 1687-1693
9. Cutforth T., and Rubin G.M. Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell 77 (1994) 1027-1036
10. Davis G.E. Affinity of integrins for damaged extracellular matrix: alpha v beta 3 binds to denatured collagen type I through RGD sites. Biochem. Biophys. Res. Commun. 182 (1992) 1025-1031
11. Dollery C.M., McEwan J.R., and Henney A.M. Matrix metalloproteinases and cardiovascular disease. Circ. Res. 77 (1995) 863-868
12. Egan S.E., Giddings B.W., Brooks M.W., Buday L., Sizeland A.M., and Weinberg R.A. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature 363 (1993) 45-51
13. Engelman J.A., Lisanti M.P., and Scherer P.E. Specific inhibitors of p38 mitogen-activated protein kinase block 3T3-L1 adipogenesis. J. Biol. Chem. 273 (1998) 32111-32120
14. Frank O., Heim M., Jakob M., Barbero A., Schafer D., Bendik I., Dick W., Heberer M., and Martin I. Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J. Cell. Biochem. 85 (2002) 737-746
15. Franklin R.A., Atherfold P.A., and McCubrey J.A. Calcium-induced ERK activation in human T lymphocytes occurs via p56(Lck) and CaM-kinase. Mol. Immunol. 37 (2000) 75-83
16. Frick K., and Bushinsky D. In vitro metabolic and respiratory acidosis selectively inhibit osteoblastic matrix gene expression. Am. J. Physiol., Renal. Physiol. 277 (1999) F750-755
17. Gomez E., Pritchard C., and Herbert T.P. cAMP-dependent protein kinase and Ca2+ influx through L-type voltage-gated calcium channels mediate Raf-independent activation of extracellular regulated kinase in response to glucagon-like peptide-1 in pancreatic beta-cells. J. Biol. Chem. 277 (2002) 48146-48151
18. Gotoh Y., Fujisawa K., Satomura K., and Nagayama M. Osteogenesis by human osteoblastic cells in diffusion chamber in vivo. Calcif. Tissue Int. 56 (1995) 246-251
19. Hagemann C., and Blank J.L. The ups and downs of MEK kinase interactions. Cell. Signal. 13 (2001) 863-875
20. Hankemeier S., Grassel S., Plenz G., Spiegel H.U., Bruckner P., and Probst A. Alteration of fracture stability influences chondrogenesis, osteogenesis and immigration of macrophages. J. Orthop. Res. 19 (2001) 531-538
21. Henle P., Zimmermann G., and Weiss S. Matrix metalloproteinases and failed fracture healing. Bone 37 (2005) 791-798
22. Hotokezaka H., Sakai E., Kanaoka K., Saito K., Matsuo K., Kitaura H., Yoshida N., and Nakayama K. U0126 and PD98059, specific inhibitors of MEK, accelerate differentiation of RAW264.7 cells into osteoclast-like cells. J. Biol. Chem. 277 (2002) 47366-47372
23. Jaiswal R.K., Jaiswal N., Bruder S.P., Mbalaviele G., Marshak D.R., and Pittenger M.F. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J. Biol. Chem. 275 (2000) 9645-9652
24. Jilka R.L., Weinstein R.S., Takahashi K., Parfitt A.M., and Manolagas S.C. Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J. Clin. Invest. 97 (1996) 1732
25. Joronen K., Salminen H., Glumoff V., Savontaus M., and Vuorio E. Temporospatial expression of tissue inhibitors of matrix metalloproteinases-1, -2 and -3 during development, growth and aging of the mouse skeleton. Histochem. Cell Biol. 114 (2000) 157-165
26. Kamei Y., Miura S., Suzuki M., Kai Y., Mizukami J., Taniguchi T., Mochida K., Hata T., Matsuda J., Aburatani H., Nishino I., and Ezaki O. Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J. Biol. Chem. 279 (2004) 41114-41123
27. Kaneki M., Kharbanda S., Pandey P., Yoshida K., Takekawa M., Liou J.R., Stone R., and Kufe D. Functional role for protein kinase Cbeta as a regulator of stress-activated protein kinase activation and monocytic differentiation of myeloid leukemia cells. Mol. Cell. Biol. 19 (1999) 461-470
28. Lawton D., Andrew J., Marsh D., Hoyland J., and Freemont A. Expression of the gene encoding the matrix gla protein by mature osteoblasts in human fracture non-unions. Mol. Pathol. 52 (1999) 92-96
29. Lecker S.H., Jagoe R.T., Gilbert A., Gomes M., Baracos V., Bailey J., Price S.R., Mitch W.E., and Goldberg A.L. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18 (2004) 39-51
30. Li Z., Yasuda Y., Li W., Bogyo M., Katz N., Gordon R.E., Fields G.B., and Bromme D. Regulation of collagenase activities of human cathepsins by glycosaminoglycans. J. Biol. Chem. 279 (2004) 5470-5479
31. Libby P. Biology of the atheromatous plaque. Proceedings of the 13th Annual Meeting of Association of Clinical Endocrinologists (2004)
32. Lindsey M.L., Goshorn D.K., Squires C.E., Escobar G.P., Hendrick J.W., Mingoia J.T., Sweterlitsch S.E., and Spinale F.G. Age-dependent changes in myocardial matrix metalloproteinase/tissue inhibitor of metalloproteinase profiles and fibroblast function. Cardiovasc. Res. 66 (2005) 410-419
33. Mauney J., and 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. 28 (2009) 251-262 (this issue)
34. Mauney J.R., Kaplan D.L., and Volloch V. Matrix-mediated retention of osteogenic differentiation potential by human adult bone marrow stromal cells during ex vivo expansion. Biomaterials 25 (2004) 3233-3243
35. Mauney J.R., Volloch V., and Kaplan D.L. Matrix-mediated retention of adipogenic differentiation potential by human adult bone marrow-derived mesenchymal stem cells during ex vivo expansion. Biomaterials 26 (2005) 6167-6175
36. Mauney J.R., Kirker-Head C., Abrahamson L., Gronowicz G., Volloch V., and 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. 79(3), 464-475. (2006)
37. Mauney J., Nguyen T., Gillen K., Kirker-Head C., Gimble J., and 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 28 (2007) 5280-5290
38. McNulty M., Spiers P., McGovern E., and Feely J. Aging is associated with increased matrix metalloproteinase-2 activity in the human aorta. Am. J. Hypertens. 18 (2005) 504-509
39. Mittelstadt P.R., Salvador J.M., Fornace A.J., and Ashwell J.D. Activating p38 MAPK: new tricks for an old kinase. Cell Cycle 4 (2005) 1189-1192
40. Muraglia A., Cancedda R., and Quartoz R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J. Cell Sci. 113 (2000) 1161-1166
41. Niu L.L., Zheng M., Cao F., Xie C., Li H.M., Yue W., Gao Y.H., Bai C.X., Zhu S.J., and Pei X.T. Migration and differentiation of exogenous rat mesenchymal stem cells engrafted into normal and injured hearts of rats. Zhonghua Yixue Zazhi 84 (2004) 38-42
42. Noon L.A., and Lloyd A.C. Hijacking the ERK signaling pathway: Mycobacterium leprae shuns MEK to drive the proliferation of infected Schwann cells. Sci. STKE 2005 (2005) 52
43. Rodriguez J.P., Montecinos L., Rios S., Reyes P., and Martinez J. Mesenchymal stem cells from osteoporotic patients produce a type I collagen-deficient extracellular matrix favoring adipogenic differentiation. J. Cell. Biochem. 79 (2000) 557-565
44. Rossert J., and de Crombrugghe B. Type I collagen: structure, synthesis, and regulation. In: Bilezikian J., Raisz L.G., and Rodan G. (Eds). Principles of Bone Biology (1996), Academic Press, San Diego, CA 127-142
45. Roughley P.J., Rauch F., and Glorieux F.H. Osteogenesis imperfecta - clinical and molecular diversity. Eur. Cell Mater. 30 (2003) 41-47
46. Rucci N., DiGiacinto C., Orru L., Millimaggi D., Baron R., and Teti A. A novel protein kinase C alpha-dependent signal to ERK1/2 activated by alphaVbeta3 integrin in osteoclasts and in Chinese hamster ovary (CHO) cells. J. Cell Sci. 118 (2005) 3263-3275
47. Ryo I. Expression of matrix Gal-protein, type I collagen and osteonectin genes in developing rat mandibular bone. Nihon Univ. Dental J. 76 (2002) 247-255
48. Salasznyk R.M., Klees R.F., Hughlock M.K., and Plopper G.E. ERK signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells on collagen I and vitronectin. Cell. Commun. Adhes. 11 (2004) 137-153
49. Sanders M.A., and Basson M.D. Collagen IV regulates Caco-2 migration and ERK activation via alpha1beta1- and alpha2beta1-integrin-dependent Src kinase activation. Am. J. Physiol.: Gasetrointest. Liver Physiol. 286 (2004) G547-557
50. Saxena M., Williams S., Tasken K., and Mustelin T. Crosstalk between cAMP-dependent kinase and MAP kinase through a protein tyrosine phosphatase. Nat. Cell Biol. 1 (1999) 305-311
51. Scheven B.A., Hamilton N.J., Farquharson C., Rucklidge G.J., and Robins S.P. Immunohistochemical localization of native and denatured collagen types I and II in fetal and adult rat long bones. Bone 9 6 (1988) 407-414
52. Schlaepfer D.D., and Hunter T. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16 (1996) 5623-5633
53. Shi G.P., Sukhova G.K., Grubb A., Ducharme A., Rhode L.H., Lee R.T., Ridker P.M., Libby P., and Chapman H.A. Cystatin C deficiency in human atherosclerosis and aortic aneurysms. J. Clin. Invest. 104 (1999) 1191-1197
54. Short S.M., Boyer J.L., and Juliano R.L. Integrins regulate the linkage between upstream and downstream events in G protein-coupled receptor signaling to mitogen-activated protein kinase. J. Biol. Chem. 275 (2000) 12970-12977
55. Sokolov B.P., Sher B.M., Hausmann J., Marik I., Deyl Z., and Kalinin V.N. Altered ratio of collagen chains in bone of a patient with non-lethal osteogenesis imperfecta. Biochim. Biophys. Acta 1138 (1992) 93-96
56. Takeuchi Y., Suzawa M., Kikuchi T., Nishida E., Fujita T., and Matsumoto T. Differentiation and transforming growth factor-beta receptor down-regulation by collagen-alpha2beta1 integrin interaction is mediated by focal adhesion kinase and its downstream signals in murine osteoblastic cells. J. Biol. Chem. 272 (1997) 29309-29316
57. Tamura S., Hanada M., Ohnishi M., Katsura K., Sasaki M., and Kobayashi T. Regulation of stress-activated protein kinase signaling pathways by protein phosphatases. Eur. J. Biochem. 269 (2002) 1060-1066
58. Tang Q.Q., Otto T.C., and Lane M.D. Mitotic clonal expansion: a synchronous process required for adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 44-49
59. Tapinos N., and Rambukkana A. Insights into regulation of human Schwann cell proliferation by Erk1/2 via a MEK-independent and p56Lck-dependent pathway from leprosy bacilli. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 9188-9193
60. Turner C.H., Owan I., Alvey T., Hulman J., and Hock J.M. Recruitment and proliferative responses of osteoblasts after mechanical loading in vivo determined using sustained-release bromodeoxyuridine. Bone 22 5 (1998) 463-469
61. Vaes G. Cellular biology and biochemical mechanism of bone resorption. A review of recent developments on the formation, activation, and mode of action of osteoclasts. Clin. Orthop. Relat. Res. 231 (1988) 239-271 (Review)
62. van der Straten A., Rommel C., Dickson B., and Hafen E. The heat shock protein 83 (Hsp83) is required for Raf-mediated signalling in Drosophila. EMBO J. 16 (1997) 1961-1969
63. Verma S., Rajaratnam J.H., Denton J., Hoyland J.A., and Byers R.J. Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J. Clin. Pathol. 55 (2002) 693
64. Volloch V., and Kaplan D. Matrix-mediated cellular rejuvenation. Matrix Biol. 21 (2002) 533-543
65. Wang M., and Lakatta E.G. Altered regulation of matrix metalloproteinase-2 in aortic remodeling during aging. Hypertension 39 (2002) 865-873
66. Wang Y., Singh A., Xu P., Pindrus M.A., and Kaplan D. Expansion and osteogenic differentiation of bone marrow-derived mesenchymal stem cells on a vitamin C functionalized polymer. Biomaterials 27 (2006) 3265-3273
67. Wary K.K., Mainiero F., Isakoff S.J., Marcantonio E.E., and Giancotti F.G. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87 (1996) 733-743
68. Wary K.K., Mariotti A., Zurzolo C., and Giancotti F.G. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94 (1998) 625-634
69. Waza M., Adachi H., Katsuno M., Minamiyama M., Sang C., Tanaka F., Inukai A., Doyu M., and Sobue G. 17-AAG, an Hsp90 inhibitor, ameliorates polyglutamine-mediated motor neuron degeneration. Nat. Med. 11 (2005) 1088-1095
70. Wen-Sheng W. Protein kinase C alpha trigger Ras and Raf-independent MEK/ERK activation for TPA-induced growth inhibition of human hepatoma cell HepG2. Cancer Lett. 239 (2005) 27-35
71. Willing M.C., Deschenes S.P., Scott D.A., Byers P.H., Slayton R.L., Pitts S.H., Arikat H., and Roberts E.J. Osteogenesis imperfecta type I: molecular heterogeneity for COL1A1 null alleles of type I collagen. Am. J. Hum. Genet. 55 (1994) 638-647
72. Xu Y., Gurusiddappa S., Rich R.L., Owens R.T., Keene D.R., Mayne R., Hook A., and Hook M. Multiple binding sites in collagen type I for the integrins alpha1beta1 and alpha2beta1. J. Biol. Chem. 275 (2000) 38981-38989
73. Yamagishi N., Ishihara K., and Hatayama T. Hsp105alpha suppresses Hsc70 chaperone activity by inhibiting Hsc70 ATPase activity. J. Biol. Chem. 279 (2004) 41727-41733
74. Yoshiyuki M. Gene expression of noncollagenous proteins in osteoblast precursor and more differentiated osteoblast cells in vitro. Nihon Univ. Dental J. 76 (2002) 447-454