Neutrophil depletion in the early inflammatory phase delayed cutaneous wound healing in older rats: Improvements due to the use of un-denatured camel whey protein

Diagnostic Pathology

Volumn 9, Issue 1, 2014, Pages

  Ebaid, Hossam ^a,b  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

^b El Minia University ^*  (Egypt)

Author keywords

Aged rat model; Inflammatory phase; Neutrophil recruitment; Whey protein; Wound healing

Indexed keywords

MILK PROTEIN; WHEY PROTEIN;

AGING; ANIMAL; ARTICLE; CAMEL; DISEASE MODEL; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INFLAMMATION; LEUKOCYTE ACTIVATION; MALE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; OXIDATIVE STRESS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WOUND HEALING;

AGING; ANIMALS; CAMELS; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MILK PROTEINS; NEUTROPHIL ACTIVATION; NEUTROPHIL INFILTRATION; NEUTROPHILS; OXIDATIVE STRESS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WOUND HEALING;

EID: 84897660937     PISSN: None     EISSN: 17461596     Source Type: Journal    
DOI: 10.1186/1746-1596-9-46     Document Type: Article

References (50)

1. Baum CL, Arpey CJ. Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg 2005, 31:674-686.
2. Khallou-Laschet J, Varthaman A, Fornasa G, Compain C, Gaston AT, Clement M, Dussiot M, Levillain O, Graff-Dubois S, Nicoletti A, Caligiuri G. Macrophage plasticity in experimental atherosclerosis. PLoS One 2010, 5:e8852. 10.1371/journal.pone.0008852, 2810335, 20111605.
3. Bullard DC, Kunkel EJ, Kubo H, Hicks MJ, Lorenzo I, Doyle NA, Doerschuk CM, Ley K, Beaudet AL. Infectious susceptibility and severe deficiency of leukocyte rolling and recruitment in E-selectin and P-selectin double mutant mice. J Exp Med 1996, 183:2329-2336. 10.1084/jem.183.5.2329, 2192541, 8642341.
4. Savill J. Apoptosis in resolution of inflammation. J Leukoc Biol 1997, 61:375-380.
5. Ashcroft GS, Horan MA, Ferguson MW. The effects of ageing on cutaneous wound healing in mammals. J Anat 1995, 187:1-26. 1167345, 7591970.
6. Ballas CB, Davidson JM. Delayed wound healing in aged rats is associated with increased collagen gel remodeling and contraction by skin fibroblasts, not with differences in apoptotic or myofibroblast cell populations. Wound Repair Regen 2001, 19:223-237.
7. Brubaker AL, Rendon JL, Ramirez L, Choudhry MA, Kovacs EJ. Reduced neutrophil chemotaxis and infiltration contributes to delayed resolution of cutaneous wound infection with advanced age. J Immunol 2013, 15:1746-1757.
8. Curry JM, Hanke ML, Piper MG, Bailey MT, Bringardner BD, Sheridan JF, Marsh CB. Social disruption induces lung inflammation. Brain Behav Immun 2010, 24:394-402. 10.1016/j.bbi.2009.10.019, 2826531, 19903521.
9. Heasman SJ, Giles KM, Ward C, Rossi A, Haslett C, Dransfield I. Cocorticoid-mediated regulation of granulocyte apoptosis and macrophage phagocytosis of apoptotic cells: implications for the resolution of inflammation. J Endocrinol 2003, 178:29-36. 10.1677/joe.0.1780029, 12844333.
10. Viswanathan K, Dhabhar FS. Stress-induced enhancement of leukocyte trafficking into sites of surgery or immune activation. Proc Natl Acad Sci USA 2005, 102:5808-5813. 10.1073/pnas.0501650102, 556309, 15817686.
11. Nishio N, Okawa Y, Sakurai H, Isobe K. Neutrophil depletion delays wound repair in aged mice. AGE 2008, 30:11-19. 10.1007/s11357-007-9043-y, 2276589, 19424869.
12. Dawes LJ, Duncan G, Wormstone IM. Age-related differences in signaling efficiency of human lens cells underpin differential wound healingresponse rates following cataract surgery. Invest Ophthalmol Vis Sci 2013, 14:333-342.
13. Lobmann R, Ambrosch A, Schultz G, Waldmann K, Schiweck S, Lehnert H. Expression of matrix-metalloproteinases and their inhibitors in the wounds of diabetic and non-diabetic patients. Diabetologia 2002, 45:1011-1016. 10.1007/s00125-002-0868-8, 12136400.
14. Lobmann R, Schultz G, Lehnert H. Proteases and the diabetic foot syndrome: mechanisms and therapeutic implications. Diabetes Care 2005, 28:461-471. 10.2337/diacare.28.2.461, 15677818.
15. Ungvari Z, Tucsek Z, Sosnowska D, Toth P, Gautam T, Podlutsky A, Csiszar A, Losonczy G, Valcarcel-Ares MN, Sonntag WE, Csiszar A. Aging-induced dysregulation of Dicer1-dependent MicroRNA expression impairs angiogenic capacity of Rat cerebromicrovascular endothelial cells. J Gerontol A Biol Sci Med Sci 2013, 68(8):877-891. 10.1093/gerona/gls242, 23239824.
16. McDonald B, Kubes P. Chemokines: sirens of neutrophil recruitment-but is It just One song?. Immuni 2010, 8:006.
17. Ebaid H, Salem A, Sayed A, Metwalli A. Whey protein enhances normal inflammatory responses during cutaneous wound healing in diabetic rats. Lipids Health Dis 2011, 10:235. 10.1186/1476-511X-10-235, 3254143, 22168406.
18. Ebaid H, Ahmed O, Mahmoud A, Ahmed R. Limiting prolonged inflammation during proliferation and remodeling phases of wound healing in streptozotocin-induced diabetic rats supplemented with camel undenatured whey protein. BMC Immunol 2013, 14:31. 10.1186/1471-2172-14-31, 3729579, 23883360.
19. Schwentker A, Yoram V, Richard W, Timothy R. Nitric oxide and wound repair: role of cytokines?. Nitric Oxide 2002, 7:1-10. 10.1016/S1089-8603(02)00002-2, 12175813.
20. Krücken J, Mehnert L, Dkhil M, El-Khadragy M, Peter W, Benten M, Mossmann H, Wunderlich F. Massive destruction of malaria-parasitized Red blood cells despite spleen closure. Infection Immunity 2005, 73:6390-6398. 10.1128/IAI.73.10.6390-6398.2005, 1230986, 16177310.
21. Huang SP, Huang CH, Shyu JF, Lee HS, Chen SG, Chan JY, Huang SM. Promotion of wound healing using adipose-derived stem cells in radiation ulcer of a rat model. J Biomedical Scie 2013, 20:51.
22. Clark KD, Lu Z, Strand MR. Regulation of melanization by glutathione in the moth Pseudoplusia includens. Insect Biochem Molecul Biol 2010, 40:460-467.
23. Okhawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979, 95:351-358. 10.1016/0003-2697(79)90738-3, 36810.
24. Zhang T, Guo P, Zhang Y, Xiong H, Yu X, Xu S, Wang X, He D, Jin X. The antidiabetic drug metformin inhibits the proliferation of bladder cancer cells in vitro and in vivo. Int J Mol Sci 2013, 18:24603-24618.
25. Barati F, Javanbakht J, Adib-Hashemi F, Hosseini F, Safaeie F, Rajabian M, Razmjoo M, Sedaghat R, Hassan A. Histopathological and clinical evaluation of Kombucha tea and Nitrofurazone on cutaneous full-thickness wounds healing in rats: an experimental study. Diag Pathol 2013, 8:120.
26. Altavilla D, Saitta A, Cucinotta D, Galeano M, Deodato B, Colonna M, Torre V, Russo G, Sardella A, Urna G, Campo GM, Cavallar V, Squadrito G, Squadrito F. Inhibition of lipid peroxidation restores impaired vascular endothelial growth factor expression and stimulates wound healing and angiogenesis in the genetically diabetic mouse. Diabetes 2001, 50:667-674. 10.2337/diabetes.50.3.667, 11246889.
27. Clark R. Cutaneous tissue repair. I. Basic biologic consideration. J Am Acad Dermatol 1985, 13:701-725. 10.1016/S0190-9622(85)70213-7, 2416789.
28. Graves DT, Nooh N, Gillen T, Davey M, Patel S, Cottrell D, Amar S. IL-1 plays a critical role in oral, but not dermal, wound healing. J Immunol 2001, 167:5316-5320.
29. Loots MA, Lamme EN, Zeegelaar J, Mekkes JR, Bos JD, Middelkoop E. Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds. J Invest Dermatol 1998, 111:850-857. 10.1046/j.1523-1747.1998.00381.x, 9804349.
30. Moore K, Ruge F, Harding KG. T lymphocytes and the lack of activated macrophages in wound margin biopsies from chronic leg ulcers. Br J Dermatol 1997, 137:188-194. 10.1046/j.1365-2133.1997.18041895.x, 9292065.
31. Devalaraja RM, Nanney LB, Du J, Qian Q, Yu Y, Devalaraja MN, Richmond A. Delayed wound healing in CXCR2 knockout mice. J Invest Dermatol 2000, 115:234-244. 10.1046/j.1523-1747.2000.00034.x, 2664868, 10951241.
32. Mori R, Kondo T, Nishie T, Ohshima T, Asano M. Impairment of skin wound healing in beta-1,4-galactosyltransferase-deficient mice with reduced leukocyte recruitment. Am J Pathol 2004, 164:1303-1314. 10.1016/S0002-9440(10)63217-8, 1615332, 15039218.
33. Miller LS, O'Connell RM, Gutierrez MA, Pietras EM, Shahangian A, Gross CE, Thirumala A, Cheung AL, Cheng G, Modlin RL. MyD88 mediatesneutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus. Immunity 2006, 24:79-91. 10.1016/j.immuni.2005.11.011, 16413925.
34. Eming SA, Krieg T, Davidson JM. Inflammation in wound repair: molecular and cellular mechanisms. J Invest Dermatol 2007, 127:514-525. 10.1038/sj.jid.5700701, 17299434.
35. Dovi JV, He LK, DiPietro LA. Accelerated wound closure in neutrophil-depleted mice. J Leukoc Biol 2003, 73:448-455. 10.1189/jlb.0802406, 12660219.
36. Reinke JM, Sorg H. Wound repair and regeneration. Eur Surg Res 2012, 49:35-43. 10.1159/000339613, 22797712.
37. Feiken E, Rømer J, Eriksen J, Lund LR. Neutrophils express tumor necrosis factor-alpha during mouse skin wound healing. J Invest Dermatol 1995, 105:120-123. 10.1111/1523-1747.ep12313429, 7615965.
38. Pierce GF. Inflammation in nonhealing diabetic wounds: the space-time continuum does matter. Am J Pathol 2001, 159:399-403. 10.1016/S0002-9440(10)61709-9, 1850546, 11485896.
39. Fülöp AK, Falus A. Possibilities and results in the wide-scale genomic analysis of inflammation. Looking for the child among many midwives. Inflamm Res 2004, 53:517-522. 10.1007/s00011-004-1293-x, 15597145.
40. Gahr M, Speer CP, Damerau B, Sawatzki G. Influence of lactoferrin on the function of human polymorphonuclear leukocytes and monocytes. J Leukoc Biol 1991, 49:427-433.
41. Machnicki M, Zimecki M, Zagulski T. Lactoferrin regulates the release of tumour necrosis factor alpha and interleukin 6 in vivo. Int J Exp Pathol 1993, 74:433-439. 2002183, 8217778.
42. Yuli I, Tomonaga A, Synderman R. Chemoattractant receptor functions in human polymorphonuclear leukocytes are divergently altered by membrane fluidizers. Proc Natl Acad Sci USA 1982, 79:5906-5910. 10.1073/pnas.79.19.5906, 347019, 6310554.
43. Lau K, Paus R, Tiede S, Day P, Bayat A. Exploring the role of stem cells in cutaneous wound healing. Exp Dermatol 2009, 18:921-933. 10.1111/j.1600-0625.2009.00942.x, 19719838.
44. Roh C, Lyle S. Cutaneous stem cells and wound healing. Pediatr Res 2006, 59:100R-103R.
45. Kondo T, Ishida Y. Molecular pathology of wound healing. Forensic Sci Int 2010, 203:93-98. 10.1016/j.forsciint.2010.07.004, 20739128.
46. Bauer SM. Angiogenesis, vasculogenesis, and induction of healing in chronic wounds. Vasc Endovasc Surg 2005, 39:293-306.
47. Arnold F, West DC. Angiogenesis in wound healing. Pharmacol Ther 1991, 52:407-422. 10.1016/0163-7258(91)90034-J, 1726477.
48. Endrich B, Menger MD. Regeneration of the microcirculation during wound healing?. Unfallchirurg 2000, 103:1006-1008. 10.1007/s001130050661, 11142874.
49. Zorgetto V, Silveira G, Oliveira-Costa J, Soave D, Soares F, Ribeiro-Silva A. The relationship between lymphatic vascular density and vascular endothelial growth factor A (VEGF-A) expression with clinical-pathological features and survival in pancreatic adenocarcinomas. Diag Pathol 2013, 8:170.
50. Sorg H, Krueger C, Vollmar B. Intravital insights in skin wound healing using the mouse dorsal skin fold chamber. J Anat 2007, 211:810-818. 10.1111/j.1469-7580.2007.00822.x, 2375850, 18005122.