The role of interleukin-10 and hyaluronan in murine fetal fibroblast function in Vitro: Implications for recapitulating fetal regenerative wound healing

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Balaji, Swathi ^a   King, Alice ^a,e   Marsh, Emily ^a,f   LeSaint, Maria ^a,e   Bhattacharya, Sukanta S ^a,e   Han, Nathaniel ^a   Dhamija, Yashu ^a,g   Ranjan, Rajeev ^a   Le, Louis D ^a   Bollyky, Paul L ^b   Crombleholme, Timothy M ^a,c   Keswani, Sundeep G ^a,d  

^a Laboratory for Regenerative Wound Healing Division of Pediatric General   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^d TEXAS CHILDREN S HOSPITAL   (United States)

^e UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^f ROSS UNIVERSITY SCHOOL OF MEDICINE   (Dominica)

^g Northeast Ohio Medical University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; HYALURONAN SYNTHASE; HYALURONIC ACID; INTERLEUKIN 10; SYNTHETASE; UNCLASSIFIED DRUG; IL10 PROTEIN, MOUSE;

ADULT; ADULT FIBROBLAST; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL INVASION; CELL METABOLISM; CELL MIGRATION; CELL STRUCTURE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FETAL FIBROBLAST; FETUS; FIBROBLAST; IN VIVO STUDY; METABOLIC RATE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PERICELLULAR MATRIX; PHENOTYPE; PROTEIN FUNCTION; REGENERATIVE WOUND HEALING; WOUND HEALING; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; FETUS DEVELOPMENT; GENETICS; IN VITRO STUDY; METABOLISM; PHYSIOLOGY;

MURINAE;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CELLS, CULTURED; EXTRACELLULAR MATRIX; FETAL DEVELOPMENT; FIBROBLASTS; HYALURONIC ACID; IN VITRO TECHNIQUES; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; WOUND HEALING;

EID: 84929105224     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124302     Document Type: Article

References (63)

1. Adzick NS, Harrison MR, Glick PL, Beckstead JH, Villa RL, Scheuenstuhl H, et al. Comparison of fetal, newborn, and adult wound healing by histologic, enzyme-histochemical, and hydroxyproline determinations. Journal of pediatric surgery. 1985; 20(4):315-9. Epub 1985/08/01. PMID: 4045654.
2. Rowlatt U. Intrauterine wound healing in a 20 week human fetus. Virchows Arch A Pathol Anat Histol. 1979; 381(3):353-61. Epub 1979/03/23. PMID: 155931.
3. Krummel TM, Nelson JM, Diegelmann RF, Lindblad WJ, Salzberg AM, Greenfield LJ, et al. Fetal response to injury in the rabbit. Journal of pediatric surgery. 1987; 22(7):640-4. Epub 1987/07/01. PMID: 3302202.
4. Longaker MT, Whitby DJ, Adzick NS, Crombleholme TM, Langer JC, Duncan BW, et al. Studies in fetal wound healing, VI. Second and early third trimester fetal wounds demonstrate rapid collagen deposition without scar formation. Journal of pediatric surgery. 1990; 25(1):63-8; discussion 8-9. Epub 1990/01/01. PMID: 2299547.
5. Mast BA, Haynes JH, Krummel TM, Cohen IK, Diegelmann RF. Ultrastructural analysis of fetal rabbit wounds. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 1997; 5(3):243- 8. Epub 1997/07/01. doi: 10.1046/j.1524-475X.1997.50308.x PMID: 16984438.
6. Leung A, Crombleholme TM, Keswani SG. Fetal wound healing: implications for minimal scar formation. Curr Opin Pediatr. 2012; 24(3):371-8. Epub 2012/05/11. doi: 10.1097/MOP.0b013e3283535790 PMID: 22572760.
7. Cowin AJ, Brosnan MP, Holmes TM, Ferguson MW. Endogenous inflammatory response to dermal wound healing in the fetal and adult mouse. Developmental dynamics: an official publication of the American Association of Anatomists. 1998; 212(3):385-93. Epub 1998/07/22. doi: 10.1002/(sici)1097-0177(199807)212:3〈385::aid-aja6〉3.0.co;2-d PMID: 9671942.
8. Liechty KW, Adzick NS, Crombleholme TM. Diminished interleukin 6 (IL-6) production during scarless human fetal wound repair. Cytokine. 2000; 12(6):671-6. Epub 2000/06/14. doi: 10.1006/cyto.1999.0598 PMID: 10843743.
9. Liechty KW, Crombleholme TM, Cass DL, Martin B, Adzick NS. Diminished interleukin-8 (IL-8) production in the fetal wound healing response. The Journal of surgical research. 1998; 77(1):80-4. Epub 1998/08/12. doi: 10.1006/jsre.1998.5345 PMID: 9698538.
10. Wulff BC, Yu L, Parent AE, Wilgus TA. Novel differences in the expression of inflammation-associated genes between mid- and late-gestational dermal fibroblasts. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2013; 21(1):103-12. Epub 2012/11/07. doi: 10.1111/j.1524-475X.2012.00860.x PMID: 23126606; PubMed Central PMCID: PMCPmc3540136.
11. Olutoye OO, Yager DR, Cohen IK, Diegelmann RF. Lower cytokine release by fetal porcine platelets: a possible explanation for reduced inflammation after fetal wounding. Journal of pediatric surgery. 1996; 31(1):91-5. Epub 1996/01/01. PMID: 8632294.
12. Mast BA, Haynes JH, Krummel TM, Diegelmann RF, Cohen IK. In vivo degradation of fetal wound hyaluronic acid results in increased fibroplasia, collagen deposition, and neovascularization. Plastic and reconstructive surgery. 1992; 89(3):503-9. Epub 1992/03/01. PMID: 1371361.
13. Mast BA, Diegelmann RF, Krummel TM, Cohen IK. Hyaluronic acid modulates proliferation, collagen and protein synthesis of cultured fetal fibroblasts. Matrix. 1993; 13(6):441-6. Epub 1993/11/01. PMID: 8309423.
14. Olutoye OO, Barone EJ, Yager DR, Uchida T, Cohen IK, Diegelmann RF. Hyaluronic acid inhibits fetal platelet function: implications in scarless healing. Journal of pediatric surgery. 1997; 32(7):1037-40. Epub 1997/07/01. PMID: 9247229.
15. Lovvorn HN 3rd, Cass DL, Sylvester KG, Yang EY, Crombleholme TM, Adzick NS, et al. Hyaluronan receptor expression increases in fetal excisional skin wounds and correlates with fibroplasia. Journal of pediatric surgery. 1998; 33(7):1062-9; discussion 9-70. Epub 1998/08/07. PMID: 9694095.
16. DePalma RL, Krummel TM, Durham LA 3rd, Michna BA, Thomas BL, Nelson JM, et al. Characterization and quantitation of wound matrix in the fetal rabbit. Matrix. 1989; 9(3):224-31. Epub 1989/06/01. PMID: 2779482.
17. Chen WY, Abatangelo G. Functions of hyaluronan in wound repair. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 1999; 7 (2):79-89. Epub 1999/05/07. PMID: 10231509.
18. Lorenz HP, Lin RY, Longaker MT, Whitby DJ, Adzick NS. The fetal fibroblast: the effector cell of scarless fetal skin repair. Plast Reconstr Surg. 1995; 96(6):1251-9; discussion 60-1. Epub 1995/11/01. PMID: 7480221.
19. Rappolee DA, Mark D, Banda MJ, Werb Z. Wound macrophages express TGF-alpha and other growth factors in vivo: analysis by mRNA phenotyping. Science. 1988; 241(4866):708-12. Epub 1988/08/05. PMID: 3041594.
20. Sandulache VC, Parekh A, Dohar JE, Hebda PA. Fetal dermal fibroblasts retain a hyperactive migratory and contractile phenotype under 2-and 3-dimensional constraints compared to normal adult fibroblasts. Tissue engineering. 2007; 13(11):2791-801. Epub 2007/09/04. doi: 10.1089/ten.2006.0412 PMID: 17764403.
21. Park JC, Park BJ, Suh H, Park BY, Rah DK. Comparative study on motility of the cultured fetal and neonatal dermal fibroblasts in extracellular matrix. Yonsei medical journal. 2001; 42(6):587-94. Epub 2001/12/26. PMID: 11754141.
22. Chen WY, Grant ME, Schor AM, Schor SL. Differences between adult and foetal fibroblasts in the regulation of hyaluronate synthesis: correlation with migratory activity. Journal of cell science. 1989; 94 (Pt 3):577-84. Epub 1989/11/01. PMID: 2632585.
23. Gosiewska A, Yi CF, Brown LJ, Cullen B, Silcock D, Geesin JC. Differential expression and regulation of extracellular matrix-associated genes in fetal and neonatal fibroblasts. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2001; 9(3):213-22. Epub 2001/07/27. PMID: 11472618.
24. Ellis I, Banyard J, Schor SL. Differential response of fetal and adult fibroblasts to cytokines: cell migration and hyaluronan synthesis. Development. 1997; 124(8):1593-600. Epub 1997/04/01. PMID: 9108375.
25. Walraven M, Gouverneur M, Middelkoop E, Beelen RH, Ulrich MM. Altered TGF-beta signaling in fetal fibroblasts: what is known about the underlying mechanisms? Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2014; 22(1):3-13. Epub 2013/10/19. doi: 10.1111/wrr.12098 PMID: 24134669.
26. Schor SL, Schor AM, Grey AM, Rushton G. Foetal and cancer patient fibroblasts produce an autocrine migration-stimulating factor not made by normal adult cells. Journal of cell science. 1988; 90 (Pt 3):391-9. Epub 1988/07/01. PMID: 3253289.
27. Weigel PH, Fuller GM, LeBoeuf RD. A model for the role of hyaluronic acid and fibrin in the early events during the inflammatory response and wound healing. Journal of theoretical biology. 1986; 119(2):219-34. Epub 1986/03/21. PMID: 3736072.
28. Longaker MT, Chiu ES, Adzick NS, Stern M, Harrison MR, Stern R. Studies in fetal wound healing. V. A prolonged presence of hyaluronic acid characterizes fetal wound fluid. Annals of surgery. 1991; 213 (4):292-6. Epub 1991/04/01. PMID: 2009010; PubMed Central PMCID: PMC1358347.
29. Longaker MT, Chiu ES, Harrison MR, Crombleholme TM, Langer JC, Duncan BW, et al. Studies in fetal wound healing. IV. Hyaluronic acid-stimulating activity distinguishes fetal wound fluid from adult wound fluid. Annals of surgery. 1989; 210(5):667-72. Epub 1989/11/01. PMID: 2818035; PubMed Central PMCID: PMC1357805.
30. Chen WY, Grant ME, Schor AM, Schor SL. Differences between adult and foetal fibroblasts in the regulation of hyaluronate synthesis: correlation with migratory activity. J Cell Sci. 1989; 94 (Pt 3):577-84. Epub 1989/11/01. PMID: 2632585.
31. Gordon A, Kozin ED, Keswani SG, Vaikunth SS, Katz AB, Zoltick PW, et al. Permissive environment in postnatal wounds induced by adenoviral-mediated overexpression of the anti-inflammatory cytokine interleukin-10 prevents scar formation. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2008; 16(1):70-9. Epub 2007/12/19. doi: 10.1111/j.1524-475X.2007.00326.x PMID: 18086289.
32. Liechty KW, Kim HB, Adzick NS, Crombleholme TM. Fetal wound repair results in scar formation in interleukin-10-deficient mice in a syngeneic murine model of scarless fetal wound repair. Journal of pediatric surgery. 2000; 35(6):866-72; discussion 72-3. Epub 2000/06/29. doi: 10.1053/jpsu.2000.6868 PMID: 10873028.
33. Gordon A, Kozin ED, Keswani SG, Vaikunth SS, Katz AB, Zoltick PW, et al. Permissive environment in postnatal wounds induced by adenoviral-mediated overexpression of the anti-inflammatory cytokine interleukin-10 prevents scar formation. Wound Repair Regen. 2008; 16(1):70-9. Epub 2007/12/19. doi: 10.1111/j.1524-475X.2007.00326.x PMID: 18086289.
34. Kieran I, Knock A, Bush J, So K,Metcalfe A, Hobson R, et al. Interleukin-10 reduces scar formation in both animal and human cutaneous wounds: results of two preclinical and phase II randomized control studies. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2013; 21(3):428-36. Epub 2013/05/01. doi: 10.1111/wrr.12043 PMID: 23627460.
35. Peranteau WH, Zhang L, Muvarak N, Badillo AT, Radu A, Zoltick PW, et al. IL-10 overexpression decreases inflammatory mediators and promotes regenerative healing in an adult model of scar formation. The Journal of investigative dermatology. 2008; 128(7):1852-60. Epub 2008/01/18. doi: 10.1038/sj.jid.5701232 PMID: 18200061.
36. Balaji S, Leung A, Le L, Dhamija Y, Lang S, Klanke C, et al. IL-10 promotes a regenerative phenotype by regulation of hyaluronan synthesis via a STAT3-dependent mechanism. Glycobiology. 2012; 22 (11):1623-. ISI:000310368700314.
37. King A, Balaji S, Le LD, Marsh E, Crombleholme TM, Keswani SG. Interleukin-10 regulates fetal extracellular matrix hyaluronan production. Journal of pediatric surgery. 2013; 48(6):1211-7. Epub 2013/07/13. doi: 10.1016/j.jpedsurg.2013.03.014 PMID: 23845609; PubMed Central PMCID: PMC3959980.
38. King A, Balaji S, Marsh E, Le LD, Shaaban AF, Crombleholme TM, et al. Interleukin-10 regulates the fetal hyaluronan-rich extracellular matrix via a STAT3-dependent mechanism. The Journal of surgical research. 2013; 184(1):671-7. Epub 2013/05/21. doi: 10.1016/j.jss.2013.04.009 PMID: 23684616; PubMed Central PMCID: PMC3759570.
39. Kakizaki I, Kojima K, Takagaki K, Endo M, Kannagi R, Ito M, et al. A novel mechanism for the inhibition of hyaluronan biosynthesis by 4-methylumbelliferone. The Journal of biological chemistry. 2004; 279 (32):33281-9. Epub 2004/06/11. doi: 10.1074/jbc.M405918200 PMID: 15190064.
40. Kultti A, Li X, Jiang P, Thompson CB, Frost GI, Shepard HM. Therapeutic targeting of hyaluronan in the tumor stroma. Cancers. 2012; 4(3):873-903. Epub 2012/01/01. doi: 10.3390/cancers4030873 PMID: 24213471; PubMed Central PMCID: PMC3712709.
41. Kultti A, Pasonen-Seppanen S, Jauhiainen M, Rilla KJ, Karna R, Pyoria E, et al. 4-Methylumbelliferone inhibits hyaluronan synthesis by depletion of cellular UDP-glucuronic acid and downregulation of hyaluronan synthase 2 and 3. Experimental cell research. 2009; 315(11):1914-23. Epub 2009/03/17. doi: 10.1016/j.yexcr.2009.03.002 PMID: 19285976.
42. Saito T, Dai T, Asano R. The hyaluronan synthesis inhibitor 4-methylumbelliferone exhibits antitumor effects against mesenchymal-like canine mammary tumor cells. Oncology letters. 2013; 5(3):1068-74. Epub 2013/02/22. doi: 10.3892/ol.2013.1124 PMID: 23426189; PubMed Central PMCID: PMC3576365.
43. Bollyky PL, Evanko SP, Wu RP, Potter-Perigo S, Long SA, Kinsella B, et al. Th1 cytokines promote T-cell binding to antigen-presenting cells via enhanced hyaluronan production and accumulation at the immune synapse. Cellular & molecular immunology. 2010; 7(3):211-20. Epub 2010/03/17. doi: 10.1038/cmi.2010.9 PMID: 20228832; PubMed Central PMCID: PMC3027489.
44. Hiramatsu K, Sasagawa S, Outani H, Nakagawa K, Yoshikawa H, Tsumaki N. Generation of hyaline cartilaginous tissue from mouse adult dermal fibroblast culture by defined factors. J Clin Invest. 2011; 121(2):640-57. Epub 2011/02/05. doi: 10.1172/JCI44605 PMID: 21293062; PubMed Central PMCID: PMC3026734.
45. Cory AH, Owen TC, Barltrop JA, Cory JG. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 1991; 3(7):207-12. Epub 1991/07/01. PMID: 1867954.
46. Yoshioka Y, Kozawa E, Urakawa H, Arai E, Futamura N, Zhuo L, et al. Suppression of hyaluronan synthesis alleviates inflammatory responses in murine arthritis and in human rheumatoid synovial fibroblasts. Arthritis and rheumatism. 2013; 65(5):1160-70. Epub 2013/01/22. doi: 10.1002/art.37861 PMID: 23335273.
47. Edward M, Quinn JA, Pasonen-Seppanen SM, McCann BA, Tammi RH. 4-Methylumbelliferone inhibits tumour cell growth and the activation of stromal hyaluronan synthesis by melanoma cell-derived factors. The British journal of dermatology. 2010; 162(6):1224-32. Epub 2010/02/19. doi: 10.1111/j.1365-2133.2010.09699.x PMID: 20163414.
48. Wang Y, Lauer ME, Anand S, Mack JA, Maytin EV. Hyaluronan synthase 2 protects skin fibroblasts against apoptosis induced by environmental stress. The Journal of biological chemistry. 2014; 289 (46):32253-65. Epub 2014/10/01. doi: 10.1074/jbc.M114.578377 PMID: 25266724; PubMed Central PMCID: PMC4231699.
49. Meran S, Thomas D, Stephens P, Martin J, Bowen T, Phillips A, et al. Involvement of hyaluronan in regulation of fibroblast phenotype. The Journal of biological chemistry. 2007; 282(35):25687-97. Epub 2007/07/06. doi: 10.1074/jbc.M700773200 PMID: 17611197.
50. Twarock S, Tammi MI, Savani RC, Fischer JW. Hyaluronan stabilizes focal adhesions, filopodia, and the proliferative phenotype in esophageal squamous carcinoma cells. The Journal of biological chemistry. 2010; 285(30):23276-84. Epub 2010/05/14. doi: 10.1074/jbc.M109.093146 PMID: 20463012; PubMed Central PMCID: PMC2906320.
51. Bullard KM, Longaker MT, Lorenz HP. Fetal Wound Healing: Current Biology. World Journal of Surgery. 2003; 27(1):54-61. PMID: 12557038
52. Moore KW, O'Garra A, de Waal Malefyt R, Vieira P, Mosmann TR. Interleukin-10. Annual review of immunology. 1993; 11:165-90. Epub 1993/01/01. doi: 10.1146/annurev.iy.11.040193.001121 PMID: 8386517.
53. Longaker MT, Chiu ES, Adzick NS, Stern M, Harrison MR, Stern R. Studies in fetal wound healing. V. A prolonged presence of hyaluronic acid characterizes fetal wound fluid. Ann Surg. 1991; 213(4):292-6. Epub 1991/04/01. PMID: 2009010; PubMed Central PMCID: PMC1358347.
54. Caskey RC, Allukian M, Lind RC, Herdrich BJ, Xu J, Radu A, et al. Lentiviral-mediated over-expression of hyaluronan synthase-1 (HAS-1) decreases the cellular inflammatory response and results in regenerative wound repair. Cell and tissue research. 2013; 351(1):117-25. Epub 2012/11/15. doi: 10.1007/s00441-012-1504-7 PMID: 23149717.
55. Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, Calabro A Jr., et al. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest. 2000; 106(3):349-60. Epub 2000/08/10. doi: 10.1172/JCI10272 PMID: 10930438; PubMed Central PMCID: PMC314332.
56. Casini P, Nardi I, Ori M. Hyaluronan is required for cranial neural crest cells migration and craniofacial development. Developmental dynamics: an official publication of the American Association of Anatomists. 2012; 241(2):294-302. Epub 2011/12/21. doi: 10.1002/dvdy.23715 PMID: 22184056.
57. Estes JM, Adzick NS, Harrison MR, Longaker MT, Stern R. Hyaluronate metabolism undergoes an ontogenic transition during fetal development: implications for scar-free wound healing. Journal of pediatric surgery. 1993; 28(10):1227-31. Epub 1993/10/01. PMID: 8263679.
58. West DC, Shaw DM, Lorenz P, Adzick NS, Longaker MT. Fibrotic healing of adult and late gestation fetal wounds correlates with increased hyaluronidase activity and removal of hyaluronan. The international journal of biochemistry & cell biology. 1997; 29(1):201-10. Epub 1997/01/01. PMID: 9076955.
59. Walter MN, Wright KT, Fuller HR, MacNeil S, Johnson WE. Mesenchymal stem cell-conditioned medium accelerates skin wound healing: an in vitro study of fibroblast and keratinocyte scratch assays. Experimental cell research. 2010; 316(7):1271-81. Epub 2010/03/09. doi: 10.1016/j.yexcr.2010.02.026 PMID: 20206158.
60. Peura M, Kaartinen I, Suomela S, Hukkanen M, Bizik J, Harjula A, et al. Improved skin wound epithelialization by topical delivery of soluble factors from fibroblast aggregates. Burns. 2012; 38(4):541-50. Epub 2011/11/25. doi: 10.1016/j.burns.2011.10.016 PMID: 22113100.
61. Estes JM, Vande Berg JS, Adzick NS, MacGillivray TE, Desmouliere A, Gabbiani G. Phenotypic and functional features of myofibroblasts in sheep fetal wounds. Differentiation. 1994; 56(3):173-81. Epub 1994/05/01. PMID: 8034132.
62. Eming SA, Werner S, Bugnon P, Wickenhauser C, Siewe L, Utermohlen O, et al. Accelerated wound closure in mice deficient for interleukin-10. The American journal of pathology. 2007; 170(1):188-202. Epub 2007/01/04. doi: 10.2353/ajpath.2007.060370 PMID: 17200193; PubMed Central PMCID: PMC1762712.
63. Hadley HS, Stanley BJ, Fritz MC, Hauptman JG, Steficek BA. Effects of a cross-linked hyaluronic acid based gel on the healing of open wounds in dogs. Veterinary surgery: VS. 2013; 42(2):161-9. Epub 2012/11/17. doi: 10.1111/j.1532-950X.2012.01048.x PMID: 23153045.