Tobacco toxins deposited on surfaces (third hand smoke) impair wound healing

Clinical Science

Volumn 130, Issue 14, 2016, Pages 1269-1284

  Dhall, Sandeep ^a   Alamat, Raquelle ^a   Castro, Anthony ^a   Sarker, Altaf H ^b   Mao, Jian Hua ^b   Chan, Alex ^a   Hang, Bo ^b   Martins Green, Manuela ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Angiogenesis; Cytokine; DNA damage; Inflammation; Reactive oxygen species and antioxidants; Toxicants

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ELASTIN; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; PLANT TOXIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; CHEMOKINE; COLLAGEN; PASSIVE SMOKING; TIMP1 PROTEIN, MOUSE; TISSUE INHIBITOR OF METALLOPROTEINASE 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ANTIOXIDANT ACTIVITY; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; DNA ISOLATION; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; IN VIVO STUDY; INFLAMMATORY CELL; LIPID PEROXIDATION; LIPID PEROXIDATION ASSAY; MOUSE; NITRATION; NONHUMAN; OXIDATIVE STRESS; PASSIVE SMOKING; PRIORITY JOURNAL; SMOKING; THIRD HAND SMOKE; TOBACCO; WOUND HEALING IMPAIRMENT; WOUND TISSUE; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CAPILLARY PERMEABILITY; METABOLISM; WOUND HEALING;

ANIMALS; CAPILLARY PERMEABILITY; CHEMOKINES; COLLAGEN; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATIVE STRESS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TOBACCO; TOBACCO SMOKE POLLUTION; WOUND HEALING;

EID: 85014060234     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20160236     Document Type: Article

References (66)

1. Guo, S. and Dipietro, L.A. (2010) Factors affecting wound healing. J. Dent. Res. 89, 219-229
2. Sen, C.K., Gordillo, G.M., Roy, S., Kirsner, R., Lambert, L., Hunt, T.K., Gottrup, F., Gurtner, G.C. and Longaker, M.T. (2009) Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair. Regen. 17, 763-771
3. Centers for Disease Control and Prevention (US), National Center for Chronic Disease Prevention and Health Promotion (US) and Office on Smoking and Health (US) (2010), How Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease, Centers for Disease Control and Prevention (US), Atlanta, GA
4. Matt, G.E., Quintana, P.J.E., Destaillats, H., Gundel, L.A., Sleiman, M., Singer, B.C., Jacob, P., Benowitz, N., Winickoff, J.P., Rehan, V. et al. (2011) Thirdhand tobacco smoke: emerging evidence and arguments for a multidisciplinary research agenda. Environ. Health Perspect. 119, 1218-1226
5. Winickoff, J.P., Friebely, J., Tanski, S.E., Sherrod, C., Matt, G.E., Hovell, M.F. and McMillen, R.C. (2009) Beliefs about the health effects of "thirdhand" smoke and home smoking bans. Pediatrics 123, e74-e79
6. Sleiman, M., Gundel, L.A., Pankow, J.F., Jacob, P., Singer, B.C. and Destaillats, H. (2010) Formation of carcinogens indoors by surface-mediated reactions of nicotine with nitrous acid, leading to potential thirdhand smoke hazards. Proc. Natl. Acad. Sci. U.S.A. 107, 6576-6581
7. Burton, A (2011) Does the smoke ever really clear? Thirdhand smoke exposure raises new concerns. Environ. Health Perspect. 119, A70-A74
8. Mosely, L.H. and Finseth, F. (1977) Cigarette smoking: impairment of digital blood flow and wound healing in the hand. Hand 9, 97-101
9. Rogers, R.L. (1983) Cigarette smoking decreases cerebral blood flow suggesting increased risk for stroke. J. Am. Med. Assoc. 250, 2796
10. Waeber, B., Schaller, M.D., Nussberger, J., Bussien, J.P., Hofbauer, K.G. and Brunner, H.R. (1984) Skin blood flow reduction induced by cigarette smoking: role of vasopressin. Am. J. Physiol. Hear Circ. Physiol. 247, H895-H901
11. Thomsen, T., Tønnesen, H. and Møller, A.M. (2009) Effect of preoperative smoking cessation interventions on postoperative complications and smoking cessation. Br. J. Surg. 96, 451-461
12. Sorensen, L.T., Karlsmark, T. and Gottrup, F. (2003) Abstinence from smoking reduces incisional wound infection: a randomized controlled trial. Ann. Surg. 238, 1-5
13. Sorensen, L.T. and Jorgensen, T Short-term pre-operative smoking cessation intervention does not affect postoperative complications in colorectal surgery: a randomized clinical trial. Color Dis 5, 347-352
14. Martins-Green, M., Adhami, N., Frankos, M., Valdez, M., Goodwin, B., Lyubovitsky, J., Dhall, S., Garcia, M., Egiebor, I., Martinez, B. et al. (2014) Cigarette smoke toxins deposited on surfaces: implications for human health. PLoS One 9, e86391
15. Dhall, S., Wijesinghe, D.S., Karim, Z.A., Castro, A., Vemana, H.P., Khasawneh, F.T., Chalfant, C.E. and Martins-Green, M. (2015) Arachidonic acid-derived signaling lipids and functions in impaired healing. Wound Repair Regen 23, 644-656
16. Petreaca, M.L., Do, D., Dhall, S., McLelland, D., Serafino, A., Lyubovitsky, J., Schiller, N. and Martins-Green, M. (2012) Deletion of a tumor necrosis superfamily gene in mice leads to impaired healing that mimics chronic wounds in humans. Wound Repair Regen 20, 353-366
17. Furda, A., H. Santos, J. and Van Houten, B. (2014) Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. Methods Mol. Biol. 1105, 419-437
18. Hang, B., Sarker, A.H., Havel, C., Saha, S., Hazra, T.K., Schick, S., Jacob, P., Rehan, V.K., Chenna, A., Sharan, D. et al. (2013) Thirdhand smoke causes DNA damage in human cells. Mutagenesis 28, 381-391
19. Dhall, S., Silva, J.P., Liu, Y., Hrynyk, M., Garcia, M., Chan, A., Lyubovitsky, J., Neufeld, R.J. and Martins-Green, M. (2015) Release of insulin from PLGA-alginate dressing stimulates regenerative healing of burn wounds in rats. Clin. Sci. (Lond) 129, 1115-1129
20. Dhall, S., Do, D., Garcia, M., Wijesinghe, D.S., Brandon, A., Kim, J., Sanchez, A., Lyubovitsky, J., Gallagher, S., Nothnagel, E.A. et al. (2014) A novel model of chronic wounds: importance of redox imbalance and biofilm-forming bacteria for establishment of chronicity. PLoS One 9, e109848
21. Dhall, S., Do, D.C., Garcia, M., Kim, J., Mirebrahim, S., Lonardi, S., Nothnagel, E.A., Schiller, N. and Martins-Green, M. (2014) Generating and reversing chronic wounds in diabetic mice by manipulating wound redox parameters. J. Diabetes Res. 2014, 562625
22. McCawley, L.J., O'Brien, P. and Hudson, L.G. (1998) Epidermal growth factor (EGF)-and scatter factor/hepatocyte growth factor (SF/HGF)mediated keratinocyte migration is coincident with induction of matrix metalloproteinase (MMP)-9. J. Cell Physiol. 176, 255-265
23. Stevens, L.J. and Page-McCaw, A. (2012) A secreted MMP is required for reepithelialization during wound healing. Mol. Biol. Cell 23, 1068-1079
24. Caley, M.P., Martins, V.L.C. and O'Toole, E.A. (2015) Metalloproteinases and wound healing. Adv. Wound Care 4, 225-234
25. Vaalamo, M., Leivo, T. and Saarialho-Kere, U. (1999) Differential expression of tissue inhibitors of metalloproteinases (TIMP-1,-2,-3, and-4) in normal and aberrant wound healing. Hum. Pathol. 30, 795-802
26. Vaalamo, M., Weckroth, M., Puolakkainen, P., Kere, J., Saarinen, P., Lauharanta, J. and Saarialho-Kere, U.K. (1996) Patterns of matrix metalloproteinase and TIMP-1 expression in chronic and normally healing human cutaneous wounds. Br. J. Dermatol. 135, 52-59
27. Ashcroft, G.S., Herrick, S.E., Tarnuzzer, R.W., Horan, M.A., Schultz, G.S. and Ferguson, M.W.J. (1997) Human ageing impairs injury-induced in vivo expression of tissue inhibitor of matrix metalloproteinases (TIMP)-1 and-2 proteins and mRNA. J. Pathol. 183, 169-176
28. Ladwig, G.P., Robson, M.C., Liu, R.A.N. and Kuhn, M.A.N.N. (2002) Ratios of activated matrix metalloproteinase-9 to tissue inhibitor of matrix metalloproteinase-1 in wound fluids are inversely correlated with healing of pressure ulcers. Wound Repair. Regen. 10, 26-37
29. Grinnell, F. and Zhu, M. (1996) Fibronectin degradation in chronic wounds depends on the relative levels of elastase, 1-proteinase inhibitor, and 2-macroglobulin. J. Invest. Dermatol. 106, 335-341
30. McCarty, S.M., Cochrane, C.A., Clegg, P.D. and Percival, S.L. (2012) The role of endogenous and exogenous enzymes in chronic wounds: a focus on the implications of aberrant levels of both host and bacterial proteases in wound healing. Wound Repair. Regen. 20, 125-136
31. Gauglitz, G.G., Song, J., Herndon, D.N., Finnerty, C.C., Boehning, D., Barral, J.M. and Jeschke, M.G. (2008) Characterization of the inflammatory response during acute and post-acute phases after severe burn. Shock 30, 503-507
32. Fivenson, D.P., Faria, D.T., Nickoloff, B.J., Poverini, P.J., Kunkel, S., Burdick, M. and Strieter, R.M. (1997) Chemokine and inflammatory cytokine changes during chronic wound healing. Wound Repair Regen 5, 310-322
33. Liu, Y., Petreaca, M. and Martins-Green, M. (2009) Cell and molecular mechanisms of insulin-induced angiogenesis. J. Cell Mol. Med. 13, 4492-4504
34. Ma, C. and Martins-Green, M. (2009) Second-hand cigarette smoke inhibits wound healing of the cornea by stimulating inflammation that delays corneal reepithelialization. Wound Repair Regen. 17, 387-396
35. Wong, L.S. and Martins-Green, M. (2004) Firsthand cigarette smoke alters fibroblast migration and survival: Implications for impaired healing. Wound Repair Regen. 12, 471-484
36. Guo, S. and Dipietro, L.A. (2010) Factors affecting wound healing. J. Dent. Res. 89, 219-229
37. Jones, J. and Triplett, R. (1992) The relationship of cigarette smoking to impaired intraoral wound healing: a review of evidence and implications for patient care. J. Oral Maxillofac. Surg. 50, 237-239
38. Hunt, T.K., Hopf, H. and Hussain, Z. (2000) Physiology of wound healing. Adv. Skin Wound Care 13 2 Suppl, 6-11
39. Asakura, T., Ishii, Y., Chibana, K. and Fukuda, T. (2004) Leukotriene D4 stimulates collagen production from myofibroblasts transformed by TGF-beta. J. Allergy Clin. Immunol. 114, 310-315
40. Inoue, M., Kratz, G., Haegerstrand, A. and Stahle-Bäckdahl, M. (1995) Collagenase expression is rapidly induced in wound-edge keratinocytes after acute injury in human skin, persists during healing, and stops at re-epithelialization. J. Invest. Dermatol. 104, 479-483
41. Gill, S.E. and Parks, W.C. (2009) Metalloproteinases and their inhibitors: regulators of wound healing. Int. J. Biochem. 40, 1334-1347
42. Mulholland, B., Tuft, S.J. and Khaw, P.T. (2005) Matrix metalloproteinase distribution during early corneal wound healing. Eye (Lond) 19, 584-588
43. Kyriakides, T.R., Wulsin, D., Skokos, E.A., Fleckman, P., Shipley, J.M., Senior, R.M. and Bornstein, P. (2009) Mice that lack matrix metalloproteinase-9 display delayed wound healing associated with delayed reepithelization and disordered collagen fibrillogenesis. Matrix Biol 28, 65-73
44. Fu, X., Kao, J.L.F., Bergt, C., Kassim, S.Y., Huq, N.P., D'Avignon, A., Parks, W.C., Mecham, R.P. and Heinecke, J.W. (2004) Oxidative cross-linking of tryptophan to glycine restrains matrix metalloproteinase activity: Specific structural motifs control protein oxidation. J. Biol. Chem. 279, 6209-6212
45. Peppin, G.J. and Weiss, S.J. (1986) Activation of the endogenous metalloproteinase, gelatinase, by triggered human neutrophils. Proc. Natl. Acad. Sci. U.S.A. 83, 4322-4326
46. Gu, Z. (2002) S-Nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297, 1186-1190
47. Raghunath, M., Bächi, T., Meuli, M., Altermatt, S., Gobet, R., Bruckner-Tuderman, L. and Steinmann, B. (1996) Fibrillin and elastin expression in skin regenerating from cultured keratinocyte autografts: morphogenesis of microfibrils begins at the dermo-epidermal junction and precedes elastic fiber formation. J. Invest. Dermatol. 1996, 1090-1095
48. Almine, J.F., Wise, S.G. and Weiss, A.S. (2012) Elastin signaling in wound repair. Birth Defects Res. C Embryo Today 96, 248-257
49. Siana, J.E., Rex, S. and Gottrup, F. (1989) The effect of cigarette smoking on wound healing. Scand. J. Plast. Reconstr. Surg. Hand Surg. 23, 207-209
50. Jorgensen, L.N., Kallehave, F., Christensen, E., Siana, J.E. and Gottrup, F. (1998) Less collagen production in smokers. Surgery 123, 450-455
51. Sherwin, M.A. and Gastwirth, C.M. (1990) Detrimental effects of cigarette smoking on lower extremity wound healing. J. Foot. Surg. 29, 84-87
52. Schäfer, M. and Werner, S. (2008) Oxidative stress in normal and impaired wound repair. Pharmacol. Res. 58, 165-171
53. Buettner, G.R. (2011) Superoxide dismutase in redox biology: the roles of superoxide and hydrogen peroxide. Anticancer Agents Med. Chem. 11, 341-346
54. Salvemini, D., Doyle, T.M. and Cuzzocrea, S. (2006) Superoxide, peroxynitrite and oxidative/nitrative stress in inflammation. Biochem. Soc. Trans. 34, 965-970, (Pt 5)
55. Sarker, A.H., Chatterjee, A., Williams, M., Lin, S., Havel, C., Jacob, P., Boldogh, I., Hazra, T.K., Talbot, P. and Hang, B. (2014) NEIL2 protects against oxidative DNA damage induced by sidestream smoke in human cells. PLoS One 9, e90261
56. Holt, P.G. (1987) Immune and inflammatory function in cigarette smokers. Thorax 42, 241-249
57. Xu, Q., Seemanapalli, S, V., Reif, K.E., Brown, C.R. and Liang, F.T. (2007) Increasing the recruitment of neutrophils to the site of infection dramatically attenuates Borrelia burgdorferi infectivity. J. Immunol. 178, 5109-5115
58. Ritzman, A.M., Hughes-Hanks, J.M., Blaho, V.a., Wax, L.E., Mitchell, W.J. and Brown, C.R. (2010) The chemokine receptor CXCR2 ligand KC (CXCL1) mediates neutrophil recruitment and is critical for development of experimental lyme arthritis and carditis. Infect. Immun. 78, 4593-4600
59. Walz, B.A., Burgener, R., Car, B., Baggiolini, M., Kunkel, S.L. and Strieter, R.M. (1991) Structure and neutrophil-activating properties of a novel inflammatory peptide (ENA-78) with homology to interleukin 8. J. Exp. Med. 174, 1355-1362
60. Roberts, A.W. (2005) G-CSF: a key regulator of neutrophil production, but that's not all!. Growth Factors 23, 33-41
61. Semerad, C.L., Liu, F., Gregory, A.D., Stumpf, K. and Link, D.C. (2002) G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood. Immunity 17, 413-423
62. Saito, M., Kiyokawa, N., Taguchi, T., Suzuki, K., Sekino, T., Mimori, K., Suzuki, T., Nakajima, H., Katagiri, Y.U., Fujimura, J. et al. (2002) Granulocyte colony-stimulating factor directly affects human monocytes and modulates cytokine secretion. Exp. Hematol. 30, 1115-1123
63. Deshmane, S.L., Kremlev, S., Amini, S. and Sawaya, B.E. (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 29, 313-326
64. Nicola, N.A. and Babon, J.J. (2015) Leukemia inhibitory factor (LIF). Cytokine Growth Factor Rev 26, 533-544
65. Engelhardt, E., Toksoy, A., Goebeler, M., Debus, S., Bröcker, E.B. and Gillitzer, R. (1998) Chemokines IL-8, GROalpha, MCP-1, IP-10, and Mig are sequentially and differentially expressed during phase-specific infiltration of leukocyte subsets in human wound healing. Am. J. Pathol. 153, 1849-1860
66. Eliceiri, B.P. and Cheresh, D.A. (2001) Adhesion events in angiogenesis. Curr. Opin. Cell Biol. 13, 563-568