Circulating progenitor cells and the expression of Cxcl12, Cxcr4 and angiopoietin-like 4 during wound healing in the murine ear
Autoři:
Clare E. Yellowley aff001; Chrisoula A. Toupadakis aff001; Natalia Vapniarsky aff002; Alice Wong aff001
Působiště autorů:
Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California Davis, Davis, California, United States of America
aff001; Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California Davis, Davis, California, United States of America
aff002
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222462
Souhrn
Migration of cells from both local and systemic sources is essential for the inflammatory and regenerative processes that occur during normal wound healing. CXCL12 is considered a critical regulator of CXCR4-positive cell migration during tissue regeneration. In this study, we investigated the expression of Cxcl12 and Cxcr4 during healing of a murine full thickness ear wound. We also investigated the expression of angiopoietin-like 4, which has been shown to participate in wound angiogenesis and reepithelialization. At time points up to 48hrs, complete blood counts were performed using automated hematology analysis, and the numbers of circulating stem and progenitor cells quantified using flow cytometry. Expression of both Cxcr4 and Angptl4 was significantly elevated within 3 days of wounding, and both were strongly expressed in cells of the epidermis. ANGPTL4 protein expression remained elevated in the epithelium through day 14. Cxcl12 expression was increased significantly at day 3, and remained elevated through day 21. Faint Cxcl12 staining was detectable in the epithelium at day 1, and thereafter staining was faint and more generalized. There were significantly fewer circulating total white blood cells and lymphocytes 1hr following ear punching. Similarly, there was a significant early (1hr) reduction in the number of circulating endothelial progenitor cells. Further studies are warranted to investigate whether ANGPTL4 and CXCL12/CXCR4 interact or synergize to facilitate cell recruitment and migration, and to potentiate reepithelialization and wound healing.
Klíčová slova:
Biology and life sciences – Anatomy – Head – Ears – Biological tissue – Epithelium – Integumentary system – Skin – Epidermis – Dermis – Cell biology – Cellular types – Animal cells – Stem cells – Blood cells – White blood cells – Neutrophils – Immune cells – Physiology – Physiological processes – Tissue repair – Wound healing – Medicine and health sciences – Immunology
Zdroje
1. Shaw TJ, Martin P. Wound repair at a glance. J Cell Sci. The Company of Biologists Ltd; 2009 Sep 15;122(Pt 18):3209–13.
2. Lee DY, Cho T-J, Lee HR, Park MS, Yoo WJ, Chung CY, et al. Distraction osteogenesis induces endothelial progenitor cell mobilization without inflammatory response in man. Bone. 2010 Mar;46(3):673–9. 19853677
3. Gill M, Dias S, Hattori K, Rivera ML, Hicklin D, Witte L, et al. Vascular trauma induces rapid but transient mobilization of VEGFR2(+)AC133(+) endothelial precursor cells. Circ Res. 2001 Feb 2;88(2):167–74. doi: 10.1161/01.res.88.2.167 11157668
4. Matsumoto T, Kuroda R, Mifune Y, Kawamoto A, Shoji T, Miwa M, et al. Circulating endothelial/skeletal progenitor cells for bone regeneration and healing. Bone. 2008 Sep;43(3):434–9. 18547890
5. Fox A, Smythe J, Fisher N, Tyler MPH, McGrouther DA, Watt SM, et al. Mobilization of endothelial progenitor cells into the circulation in burned patients. Br J Surg. John Wiley & Sons, Ltd; 2008 Feb;95(2):244–51.
6. Laing AJ, Dillon JP, Condon ET, Street JT, Wang JH, McGuinness AJ, et al. Mobilization of endothelial precursor cells: systemic vascular response to musculoskeletal trauma. J Orthop Res. 2007 Jan;25(1):44–50. doi: 10.1002/jor.20228 17001704
7. Mansilla E, Marín GH, Drago H, Sturla F, Salas E, Gardiner C, et al. Bloodstream cells phenotypically identical to human mesenchymal bone marrow stem cells circulate in large amounts under the influence of acute large skin damage: new evidence for their use in regenerative medicine. Transplant Proc. 2006 Apr;38(3):967–9. doi: 10.1016/j.transproceed.2006.02.053 16647520
8. Wang Y, Johnsen HE, Mortensen S, Bindslev L, Ripa RS, Haack-Sørensen M, et al. Changes in circulating mesenchymal stem cells, stem cell homing factor, and vascular growth factors in patients with acute ST elevation myocardial infarction treated with primary percutaneous coronary intervention. Heart. 2006 Jun;92(6):768–74. doi: 10.1136/hrt.2005.069799 16251230
9. Kumagai K, Vasanji A, Drazba JA, Butler RS, Muschler GF. Circulating cells with osteogenic potential are physiologically mobilized into the fracture healing site in the parabiotic mice model. J Orthop Res. 2008 Feb;26(2):165–75. doi: 10.1002/jor.20477 17729300
10. Zlotnik A, Yoshie O. The chemokine superfamily revisited. Immunity. 2012 May 25;36(5):705–16. doi: 10.1016/j.immuni.2012.05.008 22633458
11. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol. 2000;18:217–42. doi: 10.1146/annurev.immunol.18.1.217 10837058
12. Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells. John Wiley & Sons, Ltd; 2005 Aug;23(7):879–94.
13. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, et al. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet. 2003 Aug 30;362(9385):697–703. doi: 10.1016/S0140-6736(03)14232-8 12957092
14. Cheng X, Wang H, Zhang X, Zhao S, Zhou Z, Mu X, et al. The Role of SDF-1/CXCR4/CXCR7 in Neuronal Regeneration after Cerebral Ischemia. Front Neurosci. Frontiers; 2017;11:590.
15. Toupadakis CA, Wong A, Genetos DC, Chung DJ, Murugesh D, Anderson MJ, et al. Long-term administration of AMD3100, an antagonist of SDF-1/CXCR4 signaling, alters fracture repair. J Orthop Res. 2012 Nov;30(11):1853–9. doi: 10.1002/jor.22145 22592891
16. Goh YY, Pal M, Chong HC, Zhu P, Tan MJ, Punugu L, et al. Angiopoietin-like 4 interacts with integrins beta1 and beta5 to modulate keratinocyte migration. Am J Pathol. 2010 Dec;177(6):2791–803. doi: 10.2353/ajpath.2010.100129 20952587
17. Wilson SS, Wong A, Toupadakis CA, Yellowley CE. Expression of angiopoietin-like protein 4 at the fracture site: Regulation by hypoxia and osteoblastic differentiation. J Orthop Res. 2015 Sep;33(9):1364–73. doi: 10.1002/jor.22898 25864912
18. Pal M, Tan MJ, Huang R-L, Goh YY, Wang XL, Tang MBY, et al. Angiopoietin-like 4 regulates epidermal differentiation. Brandner JM, editor. PLoS ONE. Public Library of Science; 2011;6(9):e25377.
19. Chong HC, Chan JSK, Goh CQ, Gounko NV, Luo B, Wang X, et al. Angiopoietin-like 4 stimulates STAT3-mediated iNOS expression and enhances angiogenesis to accelerate wound healing in diabetic mice. Mol Ther. 2014 Sep;22(9):1593–604. doi: 10.1038/mt.2014.102 24903577
20. Goh YY, Pal M, Chong HC, Zhu P, Tan MJ, Punugu L, et al. Angiopoietin-like 4 interacts with matrix proteins to modulate wound healing. J Biol Chem. American Society for Biochemistry and Molecular Biology; 2010 Oct 22;285(43):32999–3009.
21. Toupadakis CA, Granick JL, Sagy M, Wong A, Ghassemi E, Chung DJ, et al. Mobilization of endogenous stem cell populations enhances fracture healing in a murine femoral fracture model. Cytotherapy. 2013 Sep;15(9):1136–47. doi: 10.1016/j.jcyt.2013.05.004 23831362
22. Okada S, Nakauchi H, Nagayoshi K, Nishikawa S, Miura Y, Suda T. In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood. 1992 Dec 15;80(12):3044–50. 1281687
23. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005 Jul 1;121(7):1109–21. doi: 10.1016/j.cell.2005.05.026 15989959
24. Sung JH, Yang H-M, Park JB, Choi G-S, Joh J-W, Kwon CH, et al. Isolation and characterization of mouse mesenchymal stem cells. Transplant Proc. 2008 Oct;40(8):2649–54. doi: 10.1016/j.transproceed.2008.08.009 18929828
25. Qian H, Le Blanc K, Sigvardsson M. Primary mesenchymal stem and progenitor cells from bone marrow lack expression of CD44 protein. J Biol Chem. American Society for Biochemistry and Molecular Biology; 2012 Jul 27;287(31):25795–807.
26. Chakroborty D, Chowdhury UR, Sarkar C, Baral R, Dasgupta PS, Basu S. Dopamine regulates endothelial progenitor cell mobilization from mouse bone marrow in tumor vascularization. J Clin Invest. American Society for Clinical Investigation; 2008 Apr;118(4):1380–9.
27. Kim H, Cho H-J, Kim S-W, Liu B, Choi YJ, Lee J, et al. CD31+ cells represent highly angiogenic and vasculogenic cells in bone marrow: novel role of nonendothelial CD31+ cells in neovascularization and their therapeutic effects on ischemic vascular disease. Circ Res. 2010 Sep 3;107(5):602–14. doi: 10.1161/CIRCRESAHA.110.218396 20634489
28. Jung SY, Choi JH, Kwon S-M, Masuda H, Asahara T, Lee Y-M. Decursin inhibits vasculogenesis in early tumor progression by suppression of endothelial progenitor cell differentiation and function. J Cell Biochem. Wiley-Blackwell; 2012 May;113(5):1478–87.
29. Jamil S, Mousavizadeh R, Roshan-Moniri M, Tebbutt SJ, McCormack RG, Duronio V, et al. Angiopoietin-like 4 Enhances the Proliferation and Migration of Tendon Fibroblasts. Med Sci Sports Exerc. 2017 Sep;49(9):1769–77. doi: 10.1249/MSS.0000000000001294 28398948
30. Dahlhoff M, Camera E, Picardo M, Zouboulis CC, Schneider MR. Angiopoietin-like 4, a protein strongly induced during sebocyte differentiation, regulates sebaceous lipogenesis but is dispensable for sebaceous gland function in vivo. J Dermatol Sci. Elsevier; 2014 Aug;75(2):148–50.
31. Quan C, Cho MK, Shao Y, Mianecki LE, Liao E, Perry D, et al. Dermal fibroblast expression of stromal cell-derived factor-1 (SDF-1) promotes epidermal keratinocyte proliferation in normal and diseased skin. Protein Cell. Higher Education Press; 2015 Dec;6(12):890–903.
32. Xu X, Zhu F, Zhang M, Zeng D, Luo D, Liu G, et al. Stromal cell-derived factor-1 enhances wound healing through recruiting bone marrow-derived mesenchymal stem cells to the wound area and promoting neovascularization. Cells Tissues Organs (Print). Karger Publishers; 2013;197(2):103–13.
33. Avniel S, Arik Z, Maly A, Sagie A, Basst HB, Yahana MD, et al. Involvement of the CXCL12/CXCR4 pathway in the recovery of skin following burns. J Invest Dermatol. 2006 Feb;126(2):468–76. doi: 10.1038/sj.jid.5700069 16385346
34. Guo R, Chai L, Chen L, Chen W, Ge L, Li X, et al. Stromal cell-derived factor 1 (SDF-1) accelerated skin wound healing by promoting the migration and proliferation of epidermal stem cells. In Vitro Cell Dev Biol Anim. Springer US; 2015 Jun;51(6):578–85.
35. Restivo TE, Mace KA, Harken AH, Young DM. Application of the chemokine CXCL12 expression plasmid restores wound healing to near normal in a diabetic mouse model. J Trauma. 2010 Aug;69(2):392–8. doi: 10.1097/TA.0b013e3181e772b0 20699749
36. Hu C, Yong X, Li C, Lü M, Liu D, Chen L, et al. CXCL12/CXCR4 axis promotes mesenchymal stem cell mobilization to burn wounds and contributes to wound repair. J Surg Res. 2013 Jul;183(1):427–34. doi: 10.1016/j.jss.2013.01.019 23462453
37. Ma X-L, Sun X-L, Wan C-Y, Ma J-X, Tian P. Significance of circulating endothelial progenitor cells in patients with fracture healing process. J Orthop Res. Wiley-Blackwell; 2012 Nov;30(11):1860–6.
38. Toupadakis CA, Wong A, Chung DJ, Yellowley CE. Enhancement of Fracture Repair by Mobilizing Endogenous Stem Cell Populations. 2011.
39. Kumar S, Wan C, Ramaswamy G, Clemens TL, Ponnazhagan S. Mesenchymal stem cells expressing osteogenic and angiogenic factors synergistically enhance bone formation in a mouse model of segmental bone defect. Mol Ther. 2010 May;18(5):1026–34. doi: 10.1038/mt.2009.315 20068549
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