Tumors alter inflammation and impair dermal wound healing in female mice

PLoS ONE

Volumn 11, Issue 8, 2016, Pages

  Pyter, Leah M ^a,b,c   Husain, Yasmin ^c   Calero, Humberto ^c   McKim, Daniel B ^a   Lin, Hsin Yun ^a,b   Godbout, Jonathan P ^a,b   Sheridan, John F ^a,b   Engeland, Christopher G ^c,d   Marucha, Phillip T ^c,e  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BONE MARROW CELL; CANCER MORTALITY; CELL COUNT; CELL INFILTRATION; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; MORBIDITY; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKINFOLD THICKNESS; WOUND CLOSURE; WOUND HEALING IMPAIRMENT; ANIMAL; C3H MOUSE; COMPLICATION; CONDITIONED MEDIUM; CYTOLOGY; DRUG EFFECTS; EXPERIMENTAL NEOPLASM; FIBROBLAST; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INTRADERMAL DRUG ADMINISTRATION; MOUTH TUMOR; NEUTROPHIL; PATHOLOGY; PHARMACOLOGY; PRIMARY CELL CULTURE; SKIN; SQUAMOUS CELL CARCINOMA; SURGICAL WOUND; TUMOR CELL LINE; WOUND HEALING;

CONDITIONED MEDIUM; CYTOKINE;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CULTURE MEDIA, CONDITIONED; CYTOKINES; FEMALE; FIBROBLASTS; GENE EXPRESSION; IMMUNITY, INNATE; INFLAMMATION; INJECTIONS, INTRADERMAL; MICE; MICE, INBRED C3H; MOUTH NEOPLASMS; NEOPLASMS, EXPERIMENTAL; NEUTROPHILS; PRIMARY CELL CULTURE; SKIN; SURGICAL WOUND; WOUND HEALING;

EID: 84984876830     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0161537     Document Type: Article

References (63)

1. Neves J, Demaria M, Campisi J, Jasper H. Of flies, mice, and men: evolutionarily conserved tissue damage responses and aging. Developmental cell. 2015; 32(1):9-18. doi: 10.1016/j.devcel.2014.11. 028 ; PubMed Central PMCID: PMC4450349.
2. Payne WG, Naidu DK, Wheeler CK, Barkoe D, Mentis M, Salas RE, et al. Wound healing in patients with cancer. Eplasty. 2008; 8:e9. Epub 2008/02/12. ; PubMed Central PMCID: PMC2206003.
3. McNees P. Skin and wound assessment and care in oncology. Semin Oncol Nurs. 2006; 22(3):130-43. Epub 2006/08/09. doi: 10.1016/j.soncn.2006.04.003 .
4. de Araujo T, Valencia I, Federman DG, Kirsner RS. Managing the patient with venous ulcers. Ann Intern Med. 2003; 138(4):326-34. Epub 2003/02/15. .
5. McNees P, Meneses KD. Pressure ulcers and other chronic wounds in patients with and patients without cancer: A retrospective, comparative analysis of healing patterns. Ostomy Wound Manage. 2007; 53(2):70-8. Epub 2007/02/13. .
6. Harreus U. Surgical errors and risks-The head and neck cancer patient. GMS current topics in otorhinolaryngology, head and neck surgery. 2013; 12:Doc04. doi: 10.3205/cto000096 ; PubMed Central PMCID: PMC3884539.
7. Maida V, Ennis M, Corban J. Wound outcomes in patients with advanced illness. International wound journal. 2012. Epub 2012/02/03. doi: 10.1111/j.1742-481X.2012.00939.x .
8. Simon A, Sofka K, Wiszniewsky G, Blaser G, Bode U, Fleischhack G. Wound care with antibacterial honey (Medihoney) in pediatric hematology-oncology. Support Care Cancer. 2006; 14(1):91-7. Epub 2005/08/03. doi: 10.1007/s00520-005-0874-8 .
9. Lawrence WT, Norton JA, Harvey AK, Gorschboth CM, Talbot TL, Grotendorst GR. Wound healing in sarcoma-bearing rats: Tumor effects on cutaneous and deep wounds. J Surg Oncol. 1987; 35(1):7-12. Epub 1987/05/01. .
10. Crawford DT, Ketcham AS. A Standard Model for Tensiometric Studies. J Surg Res. 1965; 5:265-9. .
11. Devereux DF, Thistlethwaite PA, Thibault LE, Brennan MF. Effects of tumor bearing and protein depletion on wound breaking strength in the rat. J Surg Res. 1979; 27(4):233-8. .
12. Kolokythas A. Long-Term surgical complications in the oral cancer patient: A comprehensive review. Part II. J Oral Maxillofac Res. 2010; 1(3):e2. doi: 10.5037/jomr.2010.1302
13. Gerlach MA. Wound care issues in the patient with cancer. Nurs Clin North Am. 2005; 40(2):295-323. Epub 2005/06/01. doi: 10.1016/j.cnur.2004.09.008 .
14. Kolokythas A. Long-Term surgical complications in the oral cancer patient: A comprehensive review. Part I. J Oral Maxillofac Res. 2010; 1(3):e1. doi: 10.5037/jomr.2010.1301
15. Andrews N, Griffiths C. Dental complications of head and neck radiotherapy: Part 2. Aust Dent J. 2001; 46(3):174-82. Epub 2001/11/07. .
16. Sahai SK. Perioperative assessment of the cancer patient. Best practice & research Clinical anaesthesiology. 2013; 27(4):465-80. doi: 10.1016/j.bpa.2013.10.001 .
17. Allareddy V, Karimbux NY, Dodson TB, Lee MK. Predictors of never events in patients undergoing radical dissection of cervical lymph nodes. Oral surgery, oral medicine, oral pathology and oral radiology. 2013; 115(6):710-6. doi: 10.1016/j.oooo.2012.09.004 .
18. Weber RS, Callender DL. Antibiotic prophylaxis in clean-contaminated head and neck oncologic surgery. Ann Otol Rhinol Laryngol Suppl. 1992; 155:16-20. .
19. Ogihara H, Takeuchi K, Majima Y. Risk factors of postoperative infection in head and neck surgery. Auris Nasus Larynx. 2009; 36(4):457-60. Epub 2008/12/30. doi: 10.1016/j.anl.2008.10.005 .
20. Coskun H, Erisen L, Basut O. Factors affecting wound infection rates in head and neck surgery. Otolaryngol Head Neck Surg. 2000; 123(3):328-33. doi: 10.1067/mhn.2000.105253 .
21. Duray A, Demoulin S, Hubert P, Delvenne P, Saussez S. Immune suppression in head and neck cancers: A review. Clinical & developmental immunology. 2010; 2010:701657. doi: 10.1155/2010/701657 ; PubMed Central PMCID: PMC3061296.
22. Jewett A, Head C, Cacalano NA. Emerging mechanisms of immunosuppression in oral cancers. J Dent Res. 2006; 85(12):1061-73. Epub 2006/11/24. .
23. Vasquez-Dunddel D, Pan F, Zeng Q, Gorbounov M, Albesiano E, Fu J, et al. STAT3 regulates arginase-I in myeloid-derived suppressor cells from cancer patients. J Clin Invest. 2013; 123(4):1580-9. doi: 10.1172/JCI60083 ; PubMed Central PMCID: PMC3613901.
24. Beury DW, Parker KH, Nyandjo M, Sinha P, Carter KA, Ostrand-Rosenberg S. Cross-Talk among myeloid-derived suppressor cells, macrophages, and tumor cells impacts the inflammatory milieu of solid tumors. J Leukoc Biol. 2014. doi: 10.1189/jlb.3A0414-210R .
25. Weissflog D, Kroegel C, Luttmann W, Grahmann PR, Hasse J. Leukocyte infiltration and secretion of cytokines in pleural drainage fluid after thoracic surgery: impaired cytokine response in malignancy and postoperative complications. Chest. 1999; 115(6):1604-10. Epub 1999/06/23. .
26. Park JE, Barbul A. Understanding the role of immune regulation in wound healing. Am J Surg. 2004; 187(5A):11S-6S. Epub 2004/05/19. doi: 10.1016/S0002-9610(03)00296-4 .
27. Wilgus TA. Immune cells in the healing skin wound: influential players at each stage of repair. Pharmacol Res. 2008; 58(2):112-6. Epub 2008/08/30. doi: 10.1016/j.phrs.2008.07.009 .
28. DiPietro LA, Burdick M, Low QE, Kunkel SL, Strieter RM. MIP-1alpha as a critical macrophage chemoattractant in murine wound repair. J Clin Invest. 1998; 101(8):1693-8. doi: 10.1172/JCI1020 ; PubMed Central PMCID: PMC508751.
29. Martin P, Leibovich SJ. Inflammatory cells during wound repair: The good, the bad and the ugly. Trends Cell Biol. 2005; 15(11):599-607. doi: 10.1016/j.tcb.2005.09.002 .
30. Hier MP, Black MJ, Shenouda G, Sadeghi N, Karp SE. A murine model for the immunotherapy of head and neck squamous cell carcinoma. Laryngoscope. 1995; 105(10):1077-80. Epub 1995/10/01. doi: 10. 1288/00005537-199510000-00013 .
31. Lou E, Kellman RM, Hutchison R, Shillitoe EJ. Clinical and pathological features of the murine AT-84 orthotopic model of oral cancer. Oral Dis. 2003; 9(6):305-12. Epub 2003/11/25. .
32. Vahle AK, Kerem A, Ozturk E, Bankfalvi A, Lang S, Brandau S. Optimization of an orthotopic murine model of head and neck squamous cell carcinoma in fully immunocompetent mice-role of toll-likereceptor 4 expressed on host cells. Cancer Lett. 2012; 317(2):199-206. doi: 10.1016/j.canlet.2011.11. 027 .
33. Funk GF, Karnell LH, Robinson RA, Zhen WK, Trask DK, Hoffman HT. Presentation, treatment, and outcome of oral cavity cancer: A National Cancer Data Base report. Head Neck. 2002; 24(2):165-80. .
34. Horan MP, Quan N, Subramanian SV, Strauch AR, Gajendrareddy PK, Marucha PT. Impaired wound contraction and delayed myofibroblast differentiation in restraint-stressed mice. Brain Behav Immun. 2005; 19(3):207-16. Epub 2005/03/31. doi: 10.1016/j.bbi.2004.09.004 .
35. Mercado AM, Padgett DA, Sheridan JF, Marucha PT. Altered kinetics of IL-1 alpha, IL-1 beta, and KGF-1 gene expression in early wounds of restrained mice. Brain Behav Immun. 2002; 16(2):150-62. .
36. Koh TJ, Novak ML, Mirza RE. Assessing macrophage phenotype during tissue repair. Methods Mol Biol. 2013; 1037:507-18. doi: 10.1007/978-1-62703-505-7-30 .
37. Wohleb ES, Hanke ML, Corona AW, Powell ND, Stiner LM, Bailey MT, et al. beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J Neurosci. 2011; 31(17):6277-88. Epub 2011/04/29. doi: 10.1523/JNEUROSCI.0450-11.2011 ; PubMed Central PMCID: PMC3160240.
38. Wohleb ES, Powell ND, Godbout JP, Sheridan JF. Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J Neurosci. 2013; 33(34):13820-33. Epub 2013/08/24. doi: 10.1523/JNEUROSCI.1671-13.2013 ; PubMed Central PMCID: PMC3755721.
39. Chen L, DiPietro LA. Production and function of pigment epithelium-derived factor in isolated skin keratinocytes. Exp Dermatol. 2014; 23(6):436-8. doi: 10.1111/exd.12411 ; PubMed Central PMCID: PMC4151327.
40. Liang CC, Park AY, Guan JL. In vitro scratch assay: A convenient and inexpensive method for analysis of cell migration in vitro. Nature protocols. 2007; 2(2):329-33. doi: 10.1038/nprot.2007.30 .
41. Olsen MA, Lefta M, Dietz JR, Brandt KE, Aft R, Matthews R, et al. Risk factors for surgical site infection after major breast operation. J Am Coll Surg. 2008; 207(3):326-35. Epub 2008/08/30. doi: 10.1016/j. jamcollsurg.2008.04.021 .
42. Franz MG, Steed DL, Robson MC. Optimizing healing of the acute wound by minimizing complications. Curr Probl Surg. 2007; 44(11):691-763. doi: 10.1067/j.cpsurg.2007.07.001 .
43. Haubner F, Ohmann E, Pohl F, Strutz J, Gassner HG. Wound healing after radiation therapy: review of the literature. Radiat Oncol. 2012; 7:162. doi: 10.1186/1748-717X-7-162 ; PubMed Central PMCID: PMC3504517.
44. Lawrence WT, Talbot TL, Norton JA. Preoperative or postoperative doxorubicin hydrochloride (adriamycin): which is better for wound healing? Surgery. 1986; 100(1):9-13. .
45. Chen L, Arbieva ZH, Guo S, Marucha PT, Mustoe TA, DiPietro LA. Positional differences in the wound transcriptome of skin and oral mucosa. BMC genomics. 2010; 11:471. Epub 2010/08/14. doi: 10.1186/1471-2164-11-471 ; PubMed Central PMCID: PMC3091667.
46. Engler H, Bailey MT, Engler A, Sheridan JF. Effects of repeated social stress on leukocyte distribution in bone marrow, peripheral blood and spleen. J Neuroimmunol. 2004; 148(1-2):106-15. doi: 10.1016/j. jneuroim.2003.11.011 .
47. Mandruzzato S, Solito S, Falisi E, Francescato S, Chiarion-Sileni V, Mocellin S, et al. IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J Immunol. 2009; 182(10):6562-8. doi: 10. 4049/jimmunol.0803831 .
48. Leibovich SJ, Ross R. The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol. 1975; 78(1):71-100. ; PubMed Central PMCID: PMC1915032.
49. Mirza R, DiPietro LA, Koh TJ. Selective and specific macrophage ablation is detrimental to wound healing in mice. Am J Pathol. 2009; 175(6):2454-62. doi: 10.2353/ajpath.2009.090248 ; PubMed Central PMCID: PMC2789630.
50. Martin P, D'Souza D, Martin J, Grose R, Cooper L, Maki R, et al. Wound healing in the PU.1 null mouse-Tissue repair is not dependent on inflammatory cells. Curr Biol. 2003; 13(13):1122-8. .
51. Wilgus TA. Regenerative healing in fetal skin: A review of the literature. Ostomy Wound Manage. 2007; 53(6):16-31; quiz 2-3. .
52. Dovi JV, He LK, DiPietro LA. Accelerated wound closure in neutrophil-depleted mice. J Leukoc Biol. 2003; 73(4):448-55. .
53. Goren I, Muller E, Schiefelbein D, Christen U, Pfeilschifter J, Muhl H, et al. Systemic anti-TNFalpha treatment restores diabetes-impaired skin repair in ob/ob mice by inactivation of macrophages. J Invest Dermatol. 2007; 127(9):2259-67. doi: 10.1038/sj.jid.5700842 .
54. Tymen SD, Rojas IG, Zhou X, Fang ZJ, Zhao Y, Marucha PT. Restraint stress alters neutrophil and macrophage phenotypes during wound healing. Brain Behav Immun. 2013; 28:207-17. Epub 2012/08/14doi: 10.1016/j.bbi.2012.07.013 .
55. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nature reviews Immunology. 2011; 11(11):762-74. doi: 10.1038/nri3070 ; PubMed Central PMCID: PMC3947780.
56. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nature reviews Immunology. 2008; 8(12):958-69. 10.1038/nri2448. 19029990; PubMed Central PMCID: PMC2724991. doi: 10.1038/nri2448
57. Neeman E, Ben-Eliyahu S. Surgery and stress promote cancer metastasis: new outlooks on perioperative mediating mechanisms and immune involvement. Brain Behav Immun. 2013; 30 Suppl:S32-40. doi: 10.1016/j.bbi.2012.03.006 ; PubMed Central PMCID: PMC3423506.
58. Chen L, Guo S, Ranzer MJ, DiPietro LA. Toll-like receptor 4 has an essential role in early skin wound healing. J Invest Dermatol. 2013; 133(1):258-67. Epub 2012/09/07. doi: 10.1038/jid.2012.267 ; PubMed Central PMCID: PMC3519973.
59. Kono H, Rock KL. How dying cells alert the immune system to danger. Nature reviews Immunology. 2008; 8(4):279-89. doi: 10.1038/nri2215 ; PubMed Central PMCID: PMC2763408.
60. Chakravortty D, Kumar KS. Interaction of lipopolysaccharide with human small intestinal lamina propria fibroblasts favors neutrophil migration and peripheral blood mononuclear cell adhesion by the production of proinflammatory mediators and adhesion molecules. Biochim Biophys Acta. 1999; 1453(2):261-72. .
61. Dhabhar FS, McEwen BS. Enhancing versus suppressive effects of stress hormones on skin immune function. Proc Natl Acad Sci U S A. 1999; 96(3):1059-64. .
62. Kim JW, Tsukishiro T, Johnson JT, Whiteside TL. Expression of pro-And antiapoptotic proteins in circulating CD8+ T cells of patients with squamous cell carcinoma of the head and neck. Clin Cancer Res. 2004; 10(15):5101-10. Epub 2004/08/07. doi: 10.1158/1078-0432.CCR-04-0309 .
63. Strauss L, Bergmann C, Gooding W, Johnson JT, Whiteside TL. The frequency and suppressor function of CD4+CD25highFoxp3+ T cells in the circulation of patients with squamous cell carcinoma of the head and neck. Clin Cancer Res. 2007; 13(21):6301-11. Epub 2007/11/03. doi: 10.1158/1078-0432. CCR-07-1403