Deep Tissue Injury in Development of Pressure Ulcers: A Decrease of Inflammasome Activation and Changes in Human Skin Morphology in Response to Aging and Mechanical Load

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Stojadinovic, Olivera ^a   Minkiewicz, Julia ^a   Sawaya, Andrew ^a   Bourne, Jonathan W ^b   Torzilli, Peter ^b   de Rivero Vaccari, Juan Pablo ^a   Dietrich, W Dalton ^a   Keane, Robert W ^a   Tomic Canic, Marjana ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN FIBER; CRYOPYRIN; INFLAMMASOME;

ADULT; AGING; ARTICLE; BIOMECHANICS; BODY POSITION; CLINICAL ARTICLE; CONTROLLED STUDY; DECUBITUS; DEEP TISSUE INJURY; EPIDERMIS; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; MALE; PHYSICALLY INDUCED STRESS; PHYSIOLOGICAL COMPRESSIVE STRESS; PROTEIN ACTIVATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MODIFICATION; SKIN STRUCTURE; TISSUE INJURY;

ADULT; AGING; BIOMECHANICAL PHENOMENA; CARRIER PROTEINS; COLLAGEN; DERMIS; FEMALE; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; MALE; MATERIALS TESTING; MIDDLE AGED; MODELS, BIOLOGICAL; PRESSURE; PRESSURE ULCER; SKIN; STRESS, MECHANICAL; TIME FACTORS;

EID: 84881484537     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069223     Document Type: Article

References (74)

1. Bansal C, Scott R, Stewart D, Cockerell CJ, (2005) Decubitus ulcers: a review of the literature. Int J Dermatol 44: 805-810.
2. Baumgarten M, Margolis DJ, Localio AR, Kagan SH, Lowe RA, et al. (2006) Pressure ulcers among elderly patients early in the hospital stay. J Gerontol A Biol Sci Med Sci 61: 749-754.
3. Ankrom MA, Bennett RG, Sprigle S, Langemo D, Black JM, et al. (2005) Pressure-related deep tissue injury under intact skin and the current pressure ulcer staging systems. Adv Skin Wound Care 18: 35-42.
4. Lyder CH, (2003) Pressure ulcer prevention and management. JAMA 289: 223-226.
5. Ducker A, (2002) Pressure ulcers: assessment, prevention, and compliance. Case Manager 13: 61-64 quiz 65.
6. Beckrich K, Aronovitch SA, (1999) Hospital-acquired pressure ulcers: a comparison of costs in medical vs. surgical patients. Nurs Econ 17: 263-271.
7. Services UDoHaH (2004) Guidance to Surveyors for Long Term Care Facilities.
8. Barone EJ, Yager DR, Pozez AL, Olutoye OO, Crossland MC, et al. (1998) Interleukin-1alpha and collagenase activity are elevated in chronic wounds. Plast Reconstr Surg 102: 1023-1027 discussion 1028-1029.
9. Taverna D, Nanney LB, Pollins AC, Sindona G, Caprioli R, (2011) Multiplexed molecular descriptors of pressure ulcers defined by imaging mass spectrometry. Wound Repair Regen 19: 734-744.
10. Ladwig GP, Robson MC, Liu R, Kuhn MA, Muir DF, et al. (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.
11. Bosboom EM, Bouten CV, Oomens CW, van Straaten HW, Baaijens FP, et al. (2001) Quantification and localisation of damage in rat muscles after controlled loading; a new approach to study the aetiology of pressure sores. Med Eng Phys 23: 195-200.
12. Sisco M, Liu WR, Kryger ZB, Mustoe TA, (2007) Reduced up-regulation of cytoprotective genes in rat cutaneous tissue during the second cycle of ischemia-reperfusion. Wound Repair Regen 15: 203-212.
13. Salcido R, Popescu A, Ahn C, (2007) Animal models in pressure ulcer research. J Spinal Cord Med 30: 107-116.
14. Goldstein B, Sanders J, (1998) Skin response to repetitive mechanical stress: a new experimental model in pig. Arch Phys Med Rehabil 79: 265-272.
15. de la Garza-Rodea AS, Knaan-Shanzer S, van Bekkum DW, (2011) Pressure ulcers: description of a new model and use of mesenchymal stem cells for repair. Dermatology 223: 266-284.
16. Bonomo SR, Davidson JD, Tyrone JW, Lin X, Mustoe TA, (2000) Enhancement of wound healing by hyperbaric oxygen and transforming growth factor beta3 in a new chronic wound model in aged rabbits. Arch Surg 135: 1148-1153.
17. Bronneberg D, Spiekstra SW, Cornelissen LH, Oomens CW, Gibbs S, et al. (2007) Cytokine and chemokine release upon prolonged mechanical loading of the epidermis. Exp Dermatol 16: 567-573.
18. Cornelissen LH, Bronneberg D, Bader DL, Baaijens FP, Oomens CW, (2009) The transport profile of cytokines in epidermal equivalents subjected to mechanical loading. Ann Biomed Eng 37: 1007-1018.
19. Freedberg IM, Tomic-Canic M, Komine M, Blumenberg M, (2001) Keratins and the Keratinocyte Activation Cycle. J Invest Dermatol 116: 633-640.
20. Vukelic S, Stojadinovic O, Pastar I, Rabach M, Krzyzanowska A, et al. (2011) Cortisol synthesis in epidermis is induced by IL-1 and tissue injury. J Biol Chem 286: 10265-10275.
21. Contassot E, Beer H, French L, (2012) Interleukin-1, inflammasomes, autoinflammation and the skin. Swiss Med Wkly 142: 0.
22. Feldmeyer L, Werner S, French LE, Beer HD, (2010) Interleukin-1, inflammasomes and the skin. Eur J Cell Biol 89: 638-644.
23. Dombrowski Y, Peric M, Koglin S, Kammerbauer C, Goss C, et al. (2011) Cytosolic DNA triggers inflammasome activation in keratinocytes in psoriatic lesions. Sci Transl Med 3: 82ra38.
24. Martinon F, Tschopp J, (2007) Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 14: 10-22.
25. Rajamaki K, Lappalainen J, Oorni K, Valimaki E, Matikainen S, et al. (2010) Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS One 5: e11765.
26. Salskov-Iversen ML, Johansen C, Kragballe K, Iversen L, (2011) Caspase-5 expression is upregulated in lesional psoriatic skin. J Invest Dermatol 131: 670-676.
27. Torzilli PA, Bhargava M, Chen CT, (2011) Mechanical Loading of Articular Cartilage Reduces IL-1-Induced Enzyme Expression. Cartilage 2: 364-373.
28. Torzilli PA, Grigiene R, Huang C, Friedman SM, Doty SB, et al. (1997) Characterization of cartilage metabolic response to static and dynamic stress using a mechanical explant test system. J Biomech 30: 1-9.
29. Brophy RH, Gamradt SC, Ellis SJ, Barnes RP, Rodeo SA, et al. (2009) Effect of turf toe on foot contact pressures in professional American football players. Foot Ankle Int 30: 405-409.
30. Vukelic S, Stojadinovic O, Pastar I, Vouthounis C, Krzyzanowska A, et al. (2010) Farnesyl pyrophosphate inhibits epithelialization and wound healing through the glucocorticoid receptor. J Biol Chem 285: 1980-1988.
31. Tomic-Canic M, Mamber SW, Stojadinovic O, Lee B, Radoja N, et al. (2007) Streptolysin O enhances keratinocyte migration and proliferation and promotes skin organ culture wound healing in vitro. Wound Repair Regen 15: 71-79.
32. Pastar I, Stojadinovic O, Krzyzanowska A, Barrientos S, Stuelten C, et al. (2010) Attenuation of TGFbeta Signaling Pathway in Chronic Venous Ulcers. Mol Med 16: 92-101.
33. Noorlander ML, Melis P, Jonker A, Van Noorden CJ, (2002) A quantitative method to determine the orientation of collagen fibers in the dermis. J Histochem Cytochem 50: 1469-1474.
34. Nola GT, Vistnes LM, (1980) Differential response of skin and muscle in the experimental production of pressure sores. Plast Reconstr Surg 66: 728-733.
35. Kosiak M, (1959) Etiology and pathology of ischemic ulcers. Arch Phys Med Rehabil 40: 62-69.
36. Smith AM, Malone JA, (1990) Preventing pressure ulcers in institutionalized elders: assessing the effects of small, unscheduled shifts in body position. Decubitus 3: 20-24.
37. Feldmeyer L, Keller M, Niklaus G, Hohl D, Werner S, et al. (2007) The inflammasome mediates UVB-induced activation and secretion of interleukin-1beta by keratinocytes. Curr Biol 17: 1140-1145.
38. Sjogren F, Anderson C, (2009) Sterile trauma to normal human dermis invariably induces IL1beta, IL6 and IL8 in an innate response to "danger". Acta Derm Venereol 89: 459-465.
39. Tomic-Canic M, Komine M, Freedberg IM, Blumenberg M, (1998) Epidermal signal transduction and transcription factor activation in activated keratinocytes. J Dermatol Sci 17: 167-181.
40. Tomic-Canic M, Magnus SA, Oscar MA (2004) Epidermal repair and the chronic wound. In: David T Rovee, Maibach HI, editors. The epidermis in wound healing. Boca Raton: CRC Press LLC. pp. 25-57.
41. Suter MM, Schulze K, Bergman W, Welle M, Roosje P, et al. (2009) The keratinocyte in epidermal renewal and defence. Vet Dermatol 20: 515-532.
42. Sollberger G, Strittmatter GE, Kistowska M, French LE, Beer HD, (2012) Caspase-4 is required for activation of inflammasomes. J Immunol 188: 1992-2000.
43. Dinarello CA, (2006) Interleukin 1 and interleukin 18 as mediators of inflammation and the aging process. Am J Clin Nutr 83: 447S-455S.
44. Nakamura Y, Franchi L, Kambe N, Meng G, Strober W, et al. (2012) Critical role for mast cells in interleukin-1beta-driven skin inflammation associated with an activating mutation in the nlrp3 protein. Immunity 37: 85-95.
45. Kopfnagel V, Wittmann M, Werfel T, (2011) Human keratinocytes express AIM2 and respond to dsDNA with IL-1beta secretion. Exp Dermatol 20: 1027-1029.
46. de Rivero Vaccari JP, Lotocki G, Marcillo AE, Dietrich WD, Keane RW, (2008) A molecular platform in neurons regulates inflammation after spinal cord injury. J Neurosci 28: 3404-3414.
47. de Rivero Vaccari JP, Lotocki G, Alonso OF, Bramlett HM, Dietrich WD, et al. (2009) Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J Cereb Blood Flow Metab 29: 1251-1261.
48. Abulafia DP, de Rivero Vaccari JP, Lozano JD, Lotocki G, Keane RW, et al. (2009) Inhibition of the inflammasome complex reduces the inflammatory response after thromboembolic stroke in mice. J Cereb Blood Flow Metab 29: 534-544.
49. Youm YH, Kanneganti TD, Vandanmagsar B, Zhu X, Ravussin A, et al. (2012) The NLRP3 Inflammasome Promotes Age-Related Thymic Demise and Immunosenescence. Cell Rep 1: 56-68.
50. Kauppinen A, Niskanen H, Suuronen T, Kinnunen K, Salminen A, et al. (2012) Oxidative stress activates NLRP3 inflammasomes in ARPE-19 cells-Implications for age-related macular degeneration (AMD). Immunol Lett 147: 29-33.
51. Salminen A, Ojala J, Kaarniranta K, Kauppinen A, (2012) Mitochondrial dysfunction and oxidative stress activate inflammasomes: impact on the aging process and age-related diseases. Cell Mol Life Sci 69: 2999-3013.
52. Brem H, Tomic- Canic M, Taranovskaya A, Ehlich HP, Baskin-Bay E, et al. (2003) Healing of Elderly Patients with Diabetic Foot Ulcers, Venous Stasis Ulcers, and Pressure Ulcers. Surgical Technology International pp. 161-167.
53. Foglia E, Restelli U, Napoletano AM, Coclite D, Porazzi E, et al. (2012) Pressure ulcers management: an economic evaluation. J Prev Med Hyg 53: 30-36.
54. Linder-Ganz E, Scheinowitz M, Yizhar Z, Margulies SS, Gefen A, (2007) How do normals move during prolonged wheelchair-sitting? Technol Health Care 15: 195-202.
55. Dinarello CA, (1997) Interleukin-1. Cytokine Growth Factor Rev 8: 253-265.
56. Guma M, Ronacher L, Liu-Bryan R, Takai S, Karin M, et al. (2009) Caspase 1-independent activation of interleukin-1beta in neutrophil-predominant inflammation. Arthritis Rheum 60: 3642-3650.
57. Nagarajan UM, Sikes JD, Yeruva L, Prantner D, (2012) Significant role of IL-1 signaling, but limited role of inflammasome activation, in oviduct pathology during Chlamydia muridarum genital infection. J Immunol 188: 2866-2875.
58. Pelegrin P, Barroso-Gutierrez C, Surprenant A, (2008) P2X7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J Immunol 180: 7147-7157.
59. Joosten LA, Netea MG, Fantuzzi G, Koenders MI, Helsen MM, et al. (2009) Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1beta. Arthritis Rheum 60: 3651-3662.
60. Braga IA, Pirett CC, Ribas RM, Filho PP, Filho AD, (2013) Bacterial colonization of pressure ulcers: assessment of risk for bloodstream infection and impact on patient outcomes. J Hosp Infect 83: 314-320.
61. Agha R, Ogawa R, Pietramaggiori G, Orgill DP, (2011) A review of the role of mechanical forces in cutaneous wound healing. J Surg Res 171: 700-708.
62. Qureshi AA, Ross KM, Ogawa R, Orgill DP, (2011) Shock wave therapy in wound healing. Plast Reconstr Surg 128: 721e-727e.
63. Ichioka S, Watanabe H, Sekiya N, Shibata M, Nakatsuka T, (2008) A technique to visualize wound bed microcirculation and the acute effect of negative pressure. Wound Repair Regen 16: 460-465.
64. Derrick KL, Norbury K, Kieswetter K, Skaf J, McNulty AK, (2008) Comparative analysis of global gene expression profiles between diabetic rat wounds treated with vacuum-assisted closure therapy, moist wound healing or gauze under suction. Int Wound J 5: 615-624.
65. Orgill DP, Bayer LR, (2011) Update on negative-pressure wound therapy. Plast Reconstr Surg 127 Suppl 1: 105S-115S.
66. Demiot C, Sarrazy V, Javellaud J, Gourloi L, Botelle L, et al. (2011) Erythropoietin restores C-fiber function and prevents pressure ulcer formation in diabetic mice. J Invest Dermatol 131: 2316-2322.
67. Lin F, Pandya A, Cichowski A, Modi M, Reprogle B, et al. (2010) Deep tissue injury rat model for pressure ulcer research on spinal cord injury. J Tissue Viability 19: 67-76.
68. Witkowski JA, Parish LC, (1982) Histopathology of the decubitus ulcer. J Am Acad Dermatol 6: 1014-1021.
69. Edsberg LE, (2007) Pressure ulcer tissue histology: an appraisal of current knowledge. Ostomy Wound Manage 53: 40-49.
70. Oikarinen A, (1994) Aging of the skin connective tissue: how to measure the biochemical and mechanical properties of aging dermis. Photodermatol Photoimmunol Photomed 10: 47-52.
71. Waller JM, Maibach HI, (2006) Age and skin structure and function, a quantitative approach (II): protein, glycosaminoglycan, water, and lipid content and structure. Skin Res Technol 12: 145-154.
72. Uitto J, (1986) Connective tissue biochemistry of the aging dermis. Age-related alterations in collagen and elastin. Dermatol Clin 4: 433-446.
73. Khorramizadeh MR, Tredget EE, Telasky C, Shen Q, Ghahary A, (1999) Aging differentially modulates the expression of collagen and collagenase in dermal fibroblasts. Mol Cell Biochem 194: 99-108.
74. Quan T, He T, Shao Y, Lin L, Kang S, et al. (2006) Elevated cysteine-rich 61 mediates aberrant collagen homeostasis in chronologically aged and photoaged human skin. Am J Pathol 169: 482-490.