An essential role for senescent cells in optimal wound healing through secretion of PDGF-AA

Developmental Cell

Volumn 31, Issue 6, 2014, Pages 722-733

  Demaria, Marco ^a   Ohtani, Naoko ^b   Youssef, SamehA ^c   Rodier, Francis ^a   Toussaint, Wendy ^d   Mitchell, JamesR ^d   Laberge, Remi Martin ^a   Vijg, Jan ^e   VanSteeg, Harry ^f,g   Dollé, MartijnE T ^g   Hoeijmakers, JanH J ^d   deBruin, Alain ^c   Hara, Eiji ^b   Campisi, Judith ^a,h  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b CANCER CHEMOTHERAPY CENTER   (Japan)

^c UTRECHT UNIVERSITY   (Netherlands)

^d ERASMUS MEDICAL CENTER   (Netherlands)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^g NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^h LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLATELET DERIVED GROWTH FACTOR AA; RECOMBINANT PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; PLATELET-DERIVED GROWTH FACTOR A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL AGING; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIUM CELL; FIBROBLAST; MOUSE; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; SKIN INJURY; TISSUE REPAIR; WOUND CLOSURE; WOUND HEALING; WOUND HEALING IMPAIRMENT; ANIMAL; APOPTOSIS; CHEMISTRY; CYTOLOGY; FEMALE; LUMINESCENCE; MALE; MESODERM; METABOLISM; SECRETION (PROCESS); TRANSGENE; TRANSGENIC MOUSE;

ANIMALIA;

ANIMALS; APOPTOSIS; CELL AGING; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; FEMALE; FIBROBLASTS; LUMINESCENCE; MALE; MESODERM; MICE; MICE, TRANSGENIC; MYOFIBROBLASTS; PLATELET-DERIVED GROWTH FACTOR; TRANSGENES; WOUND HEALING;

EID: 84919480323     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.11.012     Document Type: Article

References (45)

1. Baker D.J., Wijshake T., Tchkonia T., LeBrasseur N.K., Childs B.G., van de Sluis B., Kirkland J.L., van Deursen J.M. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 2011, 479:232-236.
2. Beer H.D., Longaker M.T., Werner S. Reduced expression of PDGF and PDGF receptors during impaired wound healing. J.Invest. Dermatol. 1997, 109:132-138.
3. Betsholtz C. Insight into the physiological functions of PDGF through genetic studies in mice. Cytokine Growth Factor Rev. 2004, 15:215-228.
4. Boström H., Willetts K., Pekny M., Levéen P., Lindahl P., Hedstrand H., Pekna M., Hellström M., Gebre-Medhin S., Schalling M., et al. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 1996, 85:863-873.
5. Burd C.E., Sorrentino J.A., Clark K.S., Darr D.B., Krishnamurthy J., Deal A.M., Bardeesy N., Castrillon D.H., Beach D.H., Sharpless N.E. Monitoring tumorigenesis and senescence invivo with a p16(INK4a)-luciferase model. Cell 2013, 152:340-351.
6. Campisi J. Cancer and ageing: rival demons?. Nat. Rev. Cancer 2003, 3:339-349.
7. Campisi J. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 2013, 75:685-705.
8. Collado M., Blasco M.A., Serrano M. Cellular senescence in cancer and aging. Cell 2007, 130:223-233.
9. Coppé J.P., Kauser K., Campisi J., Beauséjour C.M. Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J.Biol. Chem. 2006, 281:29568-29574.
10. Coppé J.P., Patil C.K., Rodier F., Sun Y., Muñoz D.P., Goldstein J., Nelson P.S., Desprez P.Y., Campisi J. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 2008, 6:2853-2868.
11. Coppé J.P., Desprez P.Y., Krtolica A., Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 2010, 5:99-118.
12. Coppé J.P., Patil C.K., Rodier F., Krtolica A., Beauséjour C.M., Parrinello S., Hodgson J.G., Chin K., Desprez P.Y., Campisi J. A human-like senescence-associated secretory phenotype is conserved in mouse cells dependent on physiological oxygen. PLoS ONE 2010, 5:e9188.
13. Demaria M., Giorgi C., Lebiedzinska M., Esposito G., D'Angeli L., Bartoli A., Gough D.J., Turkson J., Levy D.E., Watson C.J., et al. A STAT3-mediated metabolic switch is involved in tumour transformation and STAT3 addiction. Aging (Albany NY) 2010, 2:823-842.
14. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin invivo. Proc. Natl. Acad. Sci. USA 1995, 92:9363-9367.
15. Doukas J., Chandler L.A., Gonzalez A.M., Gu D., Hoganson D.K., Ma C., Nguyen T., Printz M.A., Nesbit M., Herlyn M., et al. Matrix immobilization enhances the tissue repair activity of growth factor gene therapy vectors. Hum. Gene Ther. 2001, 12:783-798.
16. Erusalimsky J.D., Kurz D.J. Cellular senescence invivo: its relevance in ageing and cardiovascular disease. Exp. Gerontol. 2005, 40:634-642.
17. Freund A., Orjalo A.V., Desprez P.Y., Campisi J. Inflammatory networks during cellular senescence: causes and consequences. Trends Mol. Med. 2010, 16:238-246.
18. Freund A., Laberge R.M., Demaria M., Campisi J. Lamin B1 loss is a senescence-associated biomarker. Mol. Biol. Cell 2012, 23:2066-2075.
19. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J.Pathol. 2003, 200:500-503.
20. Guo S., Dipietro L.A. Factors affecting wound healing. J.Dent. Res. 2010, 89:219-229.
21. Hayflick L., Moorhead P.S. The serial cultivation of human diploid cell strains. Exp. Cell Res. 1961, 25:585-621.
22. Jun J.I., Lau L.F. The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing. Nat. Cell Biol. 2010, 12:676-685.
23. Kim K.H., Chen C.C., Monzon R.I., Lau L.F. Matricellular protein CCN1 promotes regression of liver fibrosis through induction of cellular senescence in hepatic myofibroblasts. Mol. Cell. Biol. 2013, 33:2078-2090.
24. Krishnamurthy J., Torrice C., Ramsey M.R., Kovalev G.I., Al-Regaiey K., Su L., Sharpless N.E. Ink4a/Arf expression is a biomarker of aging. J.Clin. Invest. 2004, 114:1299-1307.
25. Krizhanovsky V., Yon M., Dickins R.A., Hearn S., Simon J., Miething C., Yee H., Zender L., Lowe S.W. Senescence of activated stellate cells limits liver fibrosis. Cell 2008, 134:657-667.
26. Krtolica A., Parrinello S., Lockett S., Desprez P.Y., Campisi J. Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc. Natl. Acad. Sci. USA 2001, 98:12072-12077.
27. Laberge R.M., Adler D., DeMaria M., Mechtouf N., Teachenor R., Cardin G.B., Desprez P.Y., Campisi J., Rodier F. Mitochondrial DNA damage induces apoptosis in senescent cells. Cell Death Dis. 2013, 4:e727.
28. Le O.N., Rodier F., Fontaine F., Coppe J.P., Campisi J., DeGregori J., Laverdière C., Kokta V., Haddad E., Beauséjour C.M. Ionizing radiation-induced long-term expression of senescence markers in mice is independent of p53 and immune status. Aging Cell 2010, 9:398-409.
29. Martin J.A., Buckwalter J.A. The role of chondrocyte senescence in the pathogenesis of osteoarthritis and in limiting cartilage repair. J.Bone Joint Surg. Am. 2003, 85-A(Suppl 2):106-110.
30. Midwood K.S., Williams L.V., Schwarzbauer J.E. Tissue repair and the dynamics of the extracellular matrix. Int. J. Biochem. Cell Biol. 2004, 36:1031-1037.
31. Muñoz-Espín D., Cañamero M., Maraver A., Gómez-López G., Contreras J., Murillo-Cuesta S., Rodríguez-Baeza A., Varela-Nieto I., Ruberte J., Collado M., Serrano M. Programmed cell senescence during mammalian embryonic development. Cell 2013, 155:1104-1118.
32. Noureddine H., Gary-Bobo G., Alifano M., Marcos E., Saker M., Vienney N., Amsellem V., Maitre B., Chaouat A., Chouaid C., et al. Pulmonary artery smooth muscle cell senescence is a pathogenic mechanism for pulmonary hypertension in chronic lung disease. Circ. Res. 2011, 109:543-553.
33. Ohtani N., Yamakoshi K., Takahashi A., Hara E. The p16INK4a-RB pathway: molecular link between cellular senescence and tumor suppression. J.Med. Invest. 2004, 51:146-153.
34. Ostman A., Heldin C.H. Involvement of platelet-derived growth factor in disease: development of specific antagonists. Adv. Cancer Res. 2001, 80:1-38.
35. Parrinello S., Coppe J.P., Krtolica A., Campisi J. Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation. J.Cell Sci. 2005, 118:485-496.
36. Pho M., Lee W., Watt D.R., Laschinger C., Simmons C.A., McCulloch C.A. Cofilin is a marker of myofibroblast differentiation in cells from porcine aortic cardiac valves. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H1767-H1778.
37. Ray P., De A., Min J.J., Tsien R.Y., Gambhir S.S. Imaging tri-fusion multimodality reporter gene expression in living subjects. Cancer Res. 2004, 64:1323-1330.
38. Ressler S., Bartkova J., Niederegger H., Bartek J., Scharffetter-Kochanek K., Jansen-Dürr P., Wlaschek M. p16INK4A is a robust invivo biomarker of cellular aging in human skin. Aging Cell 2006, 5:379-389.
39. Seluanov A., Vaidya A., Gorbunova V. Establishing primary adult fibroblast cultures from rodents. J.Vis. Exp. 2010, (44).
40. Sherr C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999, 13:1501-1512.
41. Storer M., Mas A., Robert-Moreno A., Pecoraro M., Ortells M.C., Di Giacomo V., Yosef R., Pilpel N., Krizhanovsky V., Sharpe J., Keyes W.M. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 2013, 155:1119-1130.
42. Takeuchi S., Takahashi A., Motoi N., Yoshimoto S., Tajima T., Yamakoshi K., Hirao A., Yanagi S., Fukami K., Ishikawa Y., et al. Intrinsic cooperation between p16INK4a and p21Waf1/Cip1 in the onset of cellular senescence and tumor suppression invivo. Cancer Res. 2010, 70:9381-9390.
43. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002, 3:349-363.
44. van Deursen J.M. The role of senescent cells in ageing. Nature 2014, 509:439-446.
45. Yamakoshi K., Takahashi A., Hirota F., Nakayama R., Ishimaru N., Kubo Y., Mann D.J., Ohmura M., Hirao A., Saya H., et al. Real-time invivo imaging of p16Ink4a reveals cross talk with p53. J.Cell Biol. 2009, 186:393-407.