Thrombospondin-1 and CD47 signaling regulate healing of thermal injury in mice

Matrix Biology

Volumn 37, Issue , 2014, Pages 25-34

  Soto Pantoja, David R ^a   Shih, Hubert B ^a,b   Maxhimer, Justin B ^a   Cook, Katherine L ^d   Ghosh, Arunima ^a   Isenberg, Jeffrey S ^c   Roberts, David D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

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

^d GEORGETOWN UNIVERSITY   (United States)

Author keywords

CD47; TGF 1; Thrombospondin 1; Wound healing

Indexed keywords

CD47 ANTIGEN; MESSENGER RNA; SMAD2 PROTEIN; SMAD3 PROTEIN; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1; CD47 PROTEIN, MOUSE; COLLAGEN; MORPHOLINO OLIGONUCLEOTIDE; THROMBOSPONDIN-1, MOUSE;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; GENE DELETION; IONIZING RADIATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SOFT TISSUE INJURY; THERMAL INJURY; VELOCITY; WOUND CLOSURE; WOUND HEALING; ANIMAL; BURN; C57BL MOUSE; GENETICS; IMMUNOHISTOCHEMISTRY; LASER DOPPLER FLOWMETRY; METABOLISM; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SKIN;

ANIMALS; ANTIGENS, CD47; BURNS; COLLAGEN; IMMUNOHISTOCHEMISTRY; LASER-DOPPLER FLOWMETRY; MICE; MICE, INBRED C57BL; MORPHOLINOS; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN; SMAD2 PROTEIN; SMAD3 PROTEIN; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1; WOUND HEALING;

EID: 84908313467     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.05.003     Document Type: Article

References (37)

1. Agah A., Kyriakides T.R., Lawler J., Bornstein P. The lack of thrombospondin-1 (TSP1) dictates the course of wound healing in double-TSP1/TSP2-null mice. Am. J. Pathol. 2002, 161:831-839.
2. Blais M., Parenteau-Bareil R., Cadau S., Berthod F. Concise review: tissue-engineered skin and nerve regeneration in burn treatment. Stem Cells Transl. Med. 2013, 2:545-551.
3. Bornstein P., Agah A., Kyriakides T.R. The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int. J. Biochem. Cell Biol. 2004, 36:1115-1125.
4. Cook K.L., Metheny-Barlow L.J., Tallant E.A., Gallagher P.E. Angiotensin-(1-7) reduces fibrosis in orthotopic breast tumors. Cancer Res. 2010, 70:8319-8328.
5. DiPietro L.A., Nissen N.N., Gamelli R.L., Koch A.E., Pyle J.M., Polverini P.J. Thrombospondin 1 synthesis and function in wound repair. Am. J. Pathol. 1996, 148:1851-1860.
6. Evrard S., Bluteau O., Tulliez M., Rameau P., Gonin P., Zetterberg E., Palmblad J., Bonnefoy A., Villeval J.L., Vainchenker W., Giraudier S., Wagner-Ballon O. Thrombospondin-1 is not the major activator of TGF-beta1 in thrombopoietin-induced myelofibrosis. Blood 2011, 117:246-249.
7. Hayashi H., Sakai K., Baba H., Sakai T. Thrombospondin-1 is a novel negative regulator of liver regeneration after partial hepatectomy through transforming growth factor-beta1 activation in mice. Hepatology 2012, 55:1562-1573.
8. Isenberg J.S., Ridnour L.A., Perruccio E.M., Espey M.G., Wink D.A., Roberts D.D. Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13141-13146.
9. Isenberg J.S., Ridnour L.A., Dimitry J., Frazier W.A., Wink D.A., Roberts D.D. CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1. J. Biol. Chem. 2006, 281:26069-26080.
10. Isenberg J.S., Hyodo F., Matsumoto K., Romeo M.J., Abu-Asab M., Tsokos M., Kuppusamy P., Wink D.A., Krishna M.C., Roberts D.D. Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation. Blood 2007, 109:1945-1952.
11. Isenberg J.S., Romeo M.J., Abu-Asab M., Tsokos M., Oldenborg A., Pappan L., Wink D.A., Frazier W.A., Roberts D.D. Increasing survival of ischemic tissue by targeting CD47. Circ. Res. 2007, 100:712-720.
12. Isenberg J.S., Maxhimer J.B., Hyodo F., Pendrak M.L., Ridnour L.A., DeGraff W.G., Tsokos M., Wink D.A., Roberts D.D. Thrombospondin-1 and CD47 limit cell and tissue survival of radiation injury. Am. J. Pathol. 2008, 173:1100-1112.
13. Isenberg J.S., Maxhimer J.B., Powers P., Tsokos M., Frazier W.A., Roberts D.D. Treatment of liver ischemia-reperfusion injury by limiting thrombospondin-1/CD47 signaling. Surgery 2008, 144:752-761.
14. Isenberg J.S., Pappan L.K., Romeo M.J., Abu-Asab M., Tsokos M., Wink D.A., Frazier W.A., Roberts D.D. Blockade of thrombospondin-1-CD47 interactions prevents necrosis of full thickness skin grafts. Ann. Surg. 2008, 247:180-190.
15. Isenberg J.S., Romeo M.J., Maxhimer J.B., Smedley J., Frazier W.A., Roberts D.D. Gene silencing of CD47 and antibody ligation of thrombospondin-1 enhance ischemic tissue survival in a porcine model: implications for human disease. Ann. Surg. 2008, 247:860-868.
16. Kagan R.J., Peck M.D., Ahrenholz D.H., Hickerson W.L., Holmes J.t, Korentager R., Kraatz J., Pollock K., Kotoski G. Surgical management of the burn wound and use of skin substitutes: an expert panel white paper. J. Burn Care Res. 2013, 34:e60-e79.
17. Kaur S., Martin-Manso G., Pendrak M.L., Garfield S.H., Isenberg J.S., Roberts D.D. Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J. Biol. Chem. 2010, 285:38923-38932.
18. Kaur S., Soto-Pantoja D.R., Stein E.V., Liu C., Elkahloun A.G., Pendrak M.L., Nicolae A., Singh S.P., Nie Z., Levens D., Isenberg J.S., Roberts D.D. Thrombospondin-1 signaling through CD47 inhibits self-renewal by regulating c-Myc and other stem cell transcription factors. Sci. Rep. 2013, 3:1673.
19. Lawler J., Sunday M., Thibert V., Duquette M., George E.L., Rayburn H., Hynes R.O. Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J. Clin. Invest. 1998, 101:982-992.
20. Li S.S., Liu Z., Uzunel M., Sundqvist K.G. Endogenous thrombospondin-1 is a cell-surface ligand for regulation of integrin-dependent T-lymphocyte adhesion. Blood 2006, 108:3112-3120.
21. Lindberg F.P., Bullard D.C., Caver T.E., Gresham H.D., Beaudet A.L., Brown E.J. Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 1996, 274:795-798.
22. Murphy-Ullrich J.E., Poczatek M. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev. 2000, 11:59-69.
23. Nor J.E., Dipietro L., Murphy-Ullrich J.E., Hynes R.O., Lawler J., Polverini P.J. Activation of latent TGF-beta1 by thrombospondin-1 is a major component of wound repair. Oral Biosci. Med. 2005, 2:153-161.
24. Okamoto M., Ono M., Uchiumi T., Ueno H., Kohno K., Sugimachi K., Kuwano M. Up-regulation of thrombospondin-1 gene by epidermal growth factor and transforming growth factor beta in human cancer cells - transcriptional activation and messenger RNA stabilization. Biochim. Biophys. Acta 2002, 1574:24-34.
25. Orgill D.P., Ogawa R. Current methods of burn reconstruction. Plast. Reconstr. Surg. 2013, 131:827e-836e.
26. Penn J.W., Grobbelaar A.O., Rolfe K.J. The role of the TGF-beta family in wound healing, burns and scarring: a review. Int. J. Burns Trauma 2012, 2:18-28.
27. Penttinen R.P., Kobayashi S., Bornstein P. Transforming growth factor beta increases mRNA for matrix proteins both in the presence and in the absence of changes in mRNA stability. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:1105-1108.
28. Reinke J.M., Sorg H. Wound repair and regeneration. Eur. Surg. Res. 2012, 49:35-43.
29. Roberts D.D., Miller T.W., Rogers N.M., Yao M., Isenberg J.S. The matricellular protein thrombospondin-1 globally regulates cardiovascular function and responses to stress via CD47. Matrix Biol. 2012, 31:162-169.
30. Rogers N.M., Thomson A.W., Isenberg J.S. Activation of parenchymal CD47 promotes renal ischemia-reperfusion injury. J. Am. Soc. Nephrol. 2012, 23:1538-1550.
31. Soto-Pantoja D.R., Menon J., Gallagher P.E., Tallant E.A. Angiotensin-(1-7) inhibits tumor angiogenesis in human lung cancer xenografts with a reduction in vascular endothelial growth factor. Mol. Cancer Ther. 2009, 8:1676-1683.
32. Soto-Pantoja D.R., Miller T.W., Pendrak M.L., Degraff W.G., Sullivan C., Ridnour L.A., Abu-Asab M., Wink D.A., Tsokos M., Roberts D.D. CD47 deficiency confers cell and tissue radioprotection by activation of autophagy. Autophagy 2012, 8:1628-1642.
33. Soto-Pantoja D.R., Ridnour L.A., Wink D.A., Roberts D.D. Blockade of CD47 increases survival of mice exposed to lethal total body irradiation. Sci. Rep. 2013, 3:1038.
34. Soto-Pantoja D.R., Stein E.V., Rogers N.M., Sharifi-Sanjani M., Isenberg J.S., Roberts D.D. Therapeutic opportunities for targeting the ubiquitous cell surface receptor CD47. Expert Opin. Ther. Targets 2013, 17:89-103.
35. Streit M., Velasco P., Riccardi L., Spencer L., Brown L.F., Janes L., Lange-Asschenfeldt B., Yano K., Hawighorst T., Iruela-Arispe L., Detmar M. Thrombospondin-1 suppresses wound healing and granulation tissue formation in the skin of transgenic mice. EMBO J. 2000, 19:3272-3282.
36. Sweetwyne M.T., Murphy-Ullrich J.E. Thrombospondin1 in tissue repair and fibrosis: TGF-beta-dependent and independent mechanisms. Matrix Biol. 2012, 31:178-186.
37. Young G.D., Murphy-Ullrich J.E. The tryptophan-rich motifs of the thrombospondin type 1 repeats bind VLAL motifs in the latent transforming growth factor-beta complex. J. Biol. Chem. 2004, 279:47633-47642.