Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation

Journal of Cell Biology

Volumn 164, Issue 3, 2004, Pages 441-449

  Palumbo, Roberta ^a   Sampaolesi, Maurilio ^a   De Marchis, Francesco ^a   Tonlorenzi, Rossana ^a   Colombetti, Sara ^a   Mondino, Anna ^a   Cossu, Giulio ^a,b,c   Bianchi, Marco E ^d  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b Institute of Cell Biology and Tissue Engineering   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Cell migration; Cytokine; Inflammation; Stem cell; Tissue damage

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ALPHA SARCOGLYCAN; CYTOKINE; HIGH MOBILITY GROUP B1 PROTEIN; SARCOGLYCAN; SEPHAROSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLAST CELL; CELL MIGRATION; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; ENDOTHELIUM; EXTRACELLULAR MATRIX; IN VITRO STUDY; INFLAMMATORY CELL; MESOANGIOBLAST; MOUSE; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEM CELL; TISSUE INJURY; TISSUE REGENERATION;

ANIMALS; CATTLE; CELL DIVISION; CELL MOVEMENT; CELL TRANSPLANTATION; CELLS, CULTURED; CYTOSKELETAL PROTEINS; EMBRYO; ENDOTHELIUM, VASCULAR; HMGB1 PROTEIN; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MUSCLE, SKELETAL; RECEPTORS, IMMUNOLOGIC; REGENERATION; SARCOGLYCANS; STEM CELLS;

ANIMALIA;

EID: 0842266582     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200304135     Document Type: Article

References (34)

1. Abraham, E., J. Arcaroli, A. Carmody, H. Wang, and K.J. Tracey. 2000. HMG-1 as a mediator of acute lung inflammation. J. Immunol. 165:2950-2954.
2. Agresti, A., and M.E. Bianchi. 2003. HMGB proteins and gene expression. Curr. Opin. Genet. Dev. 13:170-178.
3. Andersson, U., H. Wang, K. Palmblad, A.C. Aveberger, O. Bloom, H. Erlandsson-Harris, A. Janson, R. Kokkola, M. Zhang, H. Yang, and K.J. Tracey. 2000. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 192:565-570.
4. Bianchi, M.E. 1988. Interaction of a protein from rat liver nuclei with cruciform DNA EMBO J. 7:843-849.
5. Bianchi, M.E., and A. Manfredi. 2004. Chromatin and cell death. Biochim. Biophys. Acta. In press.
6. Bonaldi, T., F. Talamo, P. Scaffidi, D. Ferrera, A. Porto, A. Bachi, A. Rubartelli, A. Agresti, and M.E. Bianchi. 2003. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22:5551-5560.
7. Bustin, M. 1999. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19:5237-5246.
8. Calogero, S., F. Grassi, A. Aguzzi, T. Voigrländer, P. Ferrier, S. Ferrari, and M.E. Bianchi. 1999. The lack of chromosomal protein HMG1 does nor disrupt cell growth, but causes lethal hypoglycaemia in newborn mice. Nat. Genet. 22:276-280.
9. Cossu, G., and P. Bianco. 2003. Mesoangioblasts-vascular progenitors for extravascular mesodermal tissues. Curr. Opin. Genet. Dev. 13:537-542.
10. Degryse, B., T. Bonaldi, P. Scaffidi, S. Müller, M. Resnati, F. Sanvito, G. Arrigoni, and M.E. Bianchi. 2001. The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemoraxis and cytoskeleton reorganization in rat smooth muscle cells. J. Cell Biol. 152:1197-1206.
11. Esser, S., M.G. Lampugnani, M. Corada, E. Dejana, and W. Risau. 1998. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J. Cell Sci. 111:1853-1865.
12. Ferrari, G., G. Cusella-De Angelis, M. Coletta, E. Paolucci, A. Stornaiuolo, G. Cossu, and F. Mavilio. 1998. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 279:1528-1530.
13. Fiuza, C., M. Bustin, S. Talwar, M. Tropea, E. Gerstenberger, J.H. Shelhamer, and A.F. Suffredini. 2003. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood. 101:2652-2660.
14. Gardella, S., C. Andrei, D. Ferrera, L.V. Lotti, M.R. Torrisi, M.E. Bianchi, and A. Rubartelli. 2002. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep. 3:995-1001.
15. Guazzi, S., A., Strangio, A.T. Franzi, and M.E. Bianchi. 2003. HMGB1, an architectural chromatin protein and extracellular signalling factor, has a spatially and temporally restricted expression pattern in mouse brain. Gene Expr. Patterns. 3:29-33.
16. Hofmann, M.A., S. Drury, C. Fu, W. Qu, A. Taguchi, Y. Lu, C. Avila, N. Kambham, A. Bierhaus, P. Nawroth, et al. 1999. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 97:889-901.
17. Hori, O., S.D. Yan, S. Ogawa, K. Kuwabara, M. Matsumoto, D. Stern, and A.M. Schmidt. 1995. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. J. Biol. Chem. 270:25752-25761.
18. Huttunen, H.J., C. Fages, J. Kuja-Panula, A.J. Ridley, and H. Rauvala. 2002. Receptor for advanced glycation end products-binding COOH-terminal motif of amphoterin inhibits invasive migration and metastasis. Cancer Res. 62:4805-4811.
19. LaBarge, M.A., and H.M. Blau. 2002. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell. 111:589-601.
20. Lyons, A.B., and C.R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods. 171:131-137.
21. Minasi, M.G., M. Riminucci, L. De Angelis, U. Borello, B. Berarducci, A. Innocenzi, A. Caprioli, D. Sirabella, M. Baiocchi, R. De Maria, et al. 2002. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development. 129:2773-2783.
22. Müller, S., M.E. Bianchi, and S. Knapp. 2001. Thermodynamics of HMG1 interaction with duplex DNA. Biochemistry. 40:10254-10261.
23. Orlic, D., J. Kajstura, S. Chimenti, I. Jakoniuk, S.M. Anderson, B. Li, J. Pickel, R. McKay, B. Nadal-Ginard, D.M. Bodine, et al. 2001. Bone marrow cells regenerate infarcted myocardium. Nature. 410:701-705.
24. Palumbo, R., C. Gaetano, A. Antonini, G. Pompilio, E. Bracco, L. Ronnstrand, C.H. Heldin, and M.C. Capogrossi. 2002. Different effects of high and low shear stress on platelet-derived growth factor isoform release by endothelial cells: consequences for smooth muscle cell migration. Arterioscler. Thromb. Vasc. Biol. 22:405-411.
25. Ronfani, L., M. Ferraguti, L. Croci, C.E. Ovitt, H.R. Schöler, G.G. Consalez, and M.E. Bianchi. 2001. Reduced fertility and spermatogenesis defects in mice lacking chromosomal protein Hmgb2. Development. 128:1265-1273.
26. Rousseau, S., F. Houle, H. Kotanides, L. Wirte, J. Waltenberger, J. Landry, and J. Huot. 2000. Vascular endothelial growth factor (VEGF)-driven actin-based motility is mediated by VEGFR2 and requires concerted activation of stress-activated protein kinase 2 (SAPK2/p38) and geldanamycin-sensitive phosphorylation of focal adhesion kinase. J. Biol. Chem. 275:10661-10672.
27. Sampaolesi, M., Y. Torrente, A. Innocenzi, R. Tonlorenzi, G. D'Antona, M.A. Pellegrino, R. Barresi, N. Bresolin, M.G. Cusella De Angelis, K.P. Campbell, et al. 2003. Cell therapy of α-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science. 301:487-492.
28. Sappington, P.L., R. Yang, H. Yang, K.J. Tracey, R.L. Delude, and M.P. Fink. 2002. HMGB1 B box increases the permeability of Caco-2 enterocytic monolayers and impairs intestinal barrier function in mice. Gastroenterology. 123:790-802.
29. Scaffidi, P., T. Misreli, and M.E. Bianchi. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 418:191-195.
30. + stem cells restores dystrophin in mdx mice. J. Cell Biol. 152:335-348.
31. Totsugawa, T., N. Kobayashi, T. Okitsu, H. Noguchi, T. Watanabe, T. Matsumura, M. Maruyama, T. Fujiwara, M. Sakaguchi, and N. Tanaka. 2002. Lentiviral transfer of the LacZ gene into human endothelial cells and human bone marrow mesenchymal stem cells. Cell Transplant. 11:481-488.
32. Vaccari, T., M. Beltrame, S. Ferrari, and M.E. Bianchi. 1998. Hmg4, a new member of the Hmg1/2 gene family. Genomics. 49:247-252.
33. Vicario-Abejon, C., M.J. Yusta-Boyo, C. Fernandez-Moreno, and F. de Pablo. 2003. Locally born olfactory bulb stem cells proliferate in response to insulin-related factors and require endogenous insulin-like growth factor-I for differentiation into neurons and glia. J. Neurosci. 23:895-906.
34. Wang, H., O. Bloom, M. Zhang, J.M. Vishnubhakat, M. Ombrellino, J. Che, A. Frazier, H. Yang, S. Ivanova, L. Borovikova, et al. 1999. HMG-1 as a late mediator of endotoxin lethality in mice. Science. 285:248-251.