Substance P promotes wound healing in diabetes by modulating inflammation and macrophage phenotype

American Journal of Pathology

Volumn 185, Issue 6, 2015, Pages 1638-1648

  Leal, Ermelindo C ^a,b   Carvalho, Eugénia ^a,b   Tellechea, Ana ^a,b   Kafanas, Antonios ^a   Tecilazich, Francesco ^a   Kearney, Cathal ^c,d   Kuchibhotla, Sarada ^a   Auster, Michael E ^a   Kokkotou, Efi ^a   Mooney, David J ^c,e   Logerfo, Frank W ^a   Pradhan Nabzdyk, Leena ^a   Veves, Aristidis ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c HARVARD UNIVERSITY   (United States)

^d ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^e HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; GLUCOSE; INTERLEUKIN 6; MEMBRANE METALLOENDOPEPTIDASE; NEUROKININ 1 RECEPTOR; SUBSTANCE P;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DIABETIC FOOT; DISEASE COURSE; DRUG ACTIVITY; DRUG BIOAVAILABILITY; DRUG EFFECT; ENZYME DEGRADATION; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; RABBIT MODEL; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WILD TYPE; WOUND CLOSURE; WOUND HEALING; WOUND HEALING IMPAIRMENT; ANIMAL; DIABETIC NEUROPATHY; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; RABBIT; SKIN;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; INFLAMMATION; MACROPHAGES; MICE; RABBITS; RECEPTORS, NEUROKININ-1; SKIN; SUBSTANCE P; WOUND HEALING;

EID: 84929889091     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.02.011     Document Type: Article

References (42)

1. American Diabetes Association: Vital Statistics 1996 Diabetes Alexandria, VA 31
2. S. Pavlovic, M. Daniltchenko, D.J. Tobin, E. Hagen, S.P. Hunt, B.F. Klapp, P.C. Arck, and E.M. Peters Further exploring the brain-skin connection: stress worsens dermatitis via substance P-dependent neurogenic inflammation in mice J Invest Dermatol 128 2008 434 446
3. L. Pradhan, C. Nabzdyk, N.D. Andersen, F.W. LoGerfo, and A. Veves Inflammation and neuropeptides: the connection in diabetic wound healing Expert Rev Mol Med 11 2009 e2
4. T. Dinh, F. Tecilazich, A. Kafanas, J. Doupis, C. Gnardellis, E. Leal, A. Tellechea, L. Pradhan, T.E. Lyons, J.M. Giurini, and A. Veves Mechanisms involved in the development and healing of diabetic foot ulceration Diabetes 61 2012 2937 2947
5. J.E. Olerud, M.L. Usui, D. Seckin, D.S. Chiu, C.L. Haycox, I.S. Song, J.C. Ansel, and N.W. Bunnett Neutral endopeptidase expression and distribution in human skin and wounds J Invest Dermatol 112 1999 873 881
6. B. Pernow Substance P Pharmacol Rev 35 1983 85 141
7. A. Dallos, M. Kiss, H. Polyanka, A. Dobozy, L. Kemeny, and S. Husz Effects of the neuropeptides substance P, calcitonin gene-related peptide, vasoactive intestinal polypeptide and galanin on the production of nerve growth factor and inflammatory cytokines in cultured human keratinocytes Neuropeptides 40 2006 251 263
8. M. Tokuda, R. Miyamoto, T. Sakuta, S. Nagaoka, and M. Torii Substance P activates p38 mitogen-activated protein kinase to promote IL-6 induction in human dental pulp fibroblasts Connect Tissue Res 46 2005 153 158
9. P. Schratzberger, N. Reinisch, W.M. Prodinger, C.M. Kahler, B.A. Sitte, R. Bellmann, R. Fischer-Colbrie, H. Winkler, and C.J. Wiedermann Differential chemotactic activities of sensory neuropeptides for human peripheral blood mononuclear cells J Immunol 158 1997 3895 3901
10. J. Nilsson, A.M. von Euler, and C.J. Dalsgaard Stimulation of connective tissue cell growth by substance P and substance K Nature 315 1985 61 63
11. M. Ziche, L. Morbidelli, M. Pacini, P. Geppetti, G. Alessandri, and C.A. Maggi Substance P stimulates neovascularization in vivo and proliferation of cultured endothelial cells Microvasc Res 40 1990 264 278
12. P. Rameshwar, A. Poddar, G. Zhu, and P. Gascon Receptor induction regulates the synergistic effects of substance P with IL-1 and platelet-derived growth factor on the proliferation of bone marrow fibroblasts J Immunol 158 1997 3417 3424
13. H.S. Hong, J. Lee, E. Lee, Y.S. Kwon, E. Lee, W. Ahn, M.H. Jiang, J.C. Kim, and Y. Son A new role of substance P as an injury-inducible messenger for mobilization of CD29(+) stromal-like cells Nat Med 15 2009 425 435
14. M. Nakamura, M. Kawahara, N. Morishige, T. Chikama, K. Nakata, and T. Nishida Promotion of corneal epithelial wound healing in diabetic rats by the combination of a substance P-derived peptide (FGLM-NH2) and insulin-like growth factor-1 Diabetologia 46 2003 839 842
15. V. Kant, A. Gopal, D. Kumar, S. Bag, N.P. Kurade, A. Kumar, S.K. Tandan, and D. Kumar Topically applied substance P enhanced healing of open excision wound in rats Eur J Pharmacol 715 2013 345 353
16. C. Jing, W. Jia-Han, and Z. Hong-Xing Double-edged effects of neuropeptide substance P on repair of cutaneous trauma Wound Repair Regen 18 2010 319 324
17. S. Gordon, and F.O. Martinez Alternative activation of macrophages: mechanism and functions Immunity 32 2010 593 604
18. A. Sica, and A. Mantovani Macrophage plasticity and polarization: in vivo veritas J Clin Invest 122 2012 787 795
19. T. Lucas, A. Waisman, R. Ranjan, J. Roes, T. Krieg, W. Muller, A. Roers, and S.A. Eming Differential roles of macrophages in diverse phases of skin repair J Immunol 184 2010 3964 3977
20. L. Pradhan, X. Cai, S. Wu, N.D. Andersen, M. Martin, J. Malek, P. Guthrie, A. Veves, and F.W. Logerfo Gene expression of pro-inflammatory cytokines and neuropeptides in diabetic wound healing J Surg Res 167 2011 336 342
21. L. Pradhan Nabzdyk, S. Kuchibhotla, P. Guthrie, M. Chun, M.E. Auster, C. Nabzdyk, S. Deso, N. Andersen, C. Gnardellis, F.W. LoGerfo, and A. Veves Expression of neuropeptides and cytokines in a rabbit model of diabetic neuroischemic wound healing J Vasc Surg 58 2013 766 775.e12
22. V. Falanga Wound healing and its impairment in the diabetic foot Lancet 366 2005 1736 1743
23. A.J. Singer, and R.A. Clark Cutaneous wound healing N Engl J Med 341 1999 738 746
24. M.M. Santoro, and G. Gaudino Cellular and molecular facets of keratinocyte reepithelization during wound healing Exp Cell Res 304 2005 274 286
25. M.A. Loots, E.N. Lamme, J. Zeegelaar, J.R. Mekkes, J.D. Bos, and E. Middelkoop Differences in cellular infiltrate and extracellular matrix of chronic diabetic and venous ulcers versus acute wounds J Invest Dermatol 111 1998 850 857
26. H. Brem, and M. Tomic-Canic Cellular and molecular basis of wound healing in diabetes J Clin Invest 117 2007 1219 1222
27. R.M. Gallucci, P.P. Simeonova, J.M. Matheson, C. Kommineni, J.L. Guriel, T. Sugawara, and M.I. Luster Impaired cutaneous wound healing in interleukin-6-deficient and immunosuppressed mice FASEB J 14 2000 2525 2531
28. I. Goren, E. Muller, D. Schiefelbein, U. Christen, J. Pfeilschifter, H. Muhl, and S. Frank Systemic anti-TNFalpha treatment restores diabetes-impaired skin repair in ob/ob mice by inactivation of macrophages J Invest Dermatol 127 2007 2259 2267
29. R.E. Mirza, M.M. Fang, W.J. Ennis, and T.J. Koh Blocking interleukin-1beta induces a healing-associated wound macrophage phenotype and improves healing in type 2 diabetes Diabetes 62 2013 2579 2587
30. A. Sindrilaru, T. Peters, S. Wieschalka, C. Baican, A. Baican, H. Peter, A. Hainzl, S. Schatz, Y. Qi, A. Schlecht, J.M. Weiss, M. Wlaschek, C. Sunderkotter, and K. Scharffetter-Kochanek An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice J Clin Invest 121 2011 985 997
31. S.P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R.L. Leibel, and A.W. Ferrante Jr. Obesity is associated with macrophage accumulation in adipose tissue J Clin Invest 112 2003 1796 1808
32. A.M. Saeed, S. Duffort, D. Ivanov, H. Wang, J.M. Laird, R.G. Salomon, F. Cruz-Guilloty, and V.L. Perez The oxidative stress product carboxyethylpyrrole potentiates TLR2/TLR1 inflammatory signaling in macrophages PLoS One 9 2014 e106421
33. L. Yang, G. Di, X. Qi, M. Qu, Y. Wang, H. Duan, P. Danielson, L. Xie, and Q. Zhou Substance P promotes diabetic corneal epithelial wound healing through molecular mechanisms mediated via the neurokinin-1 receptor Diabetes 63 2014 4262 4274
34. A.N. Moor, D.J. Vachon, and L.J. Gould Proteolytic activity in wound fluids and tissues derived from chronic venous leg ulcers Wound Repair Regen 17 2009 832 839
35. Y. Liu, D. Min, T. Bolton, V. Nube, S.M. Twigg, D.K. Yue, and S.V. McLennan Increased matrix metalloproteinase-9 predicts poor wound healing in diabetic foot ulcers Diabetes Care 32 2009 117 119
36. R. Lobmann, A. Ambrosch, G. Schultz, K. Waldmann, S. Schiweck, and H. Lehnert Expression of matrix-metalloproteinases and their inhibitors in the wounds of diabetic and non-diabetic patients Diabetologia 45 2002 1011 1016
37. E.A. Rayment, Z. Upton, and G.K. Shooter Increased matrix metalloproteinase-9 (MMP-9) activity observed in chronic wound fluid is related to the clinical severity of the ulcer Br J Dermatol 158 2008 951 961
38. C.L. Baum, and C.J. Arpey Normal cutaneous wound healing: clinical correlation with cellular and molecular events Dermatol Surg 31 2005 674 686 discussion 86
39. B.C. Tieu, C. Lee, H. Sun, W. Lejeune, A. Recinos 3rd, X. Ju, H. Spratt, D.C. Guo, D. Milewicz, R.G. Tilton, and A.R. Brasier An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice J Clin Invest 119 2009 3637 3651
40. B. Hinz, D. Mastrangelo, C.E. Iselin, C. Chaponnier, and G. Gabbiani Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation Am J Pathol 159 2001 1009 1020
41. M.L. Spenny, P. Muangman, S.R. Sullivan, N.W. Bunnett, J.C. Ansel, J.E. Olerud, and N.S. Gibran Neutral endopeptidase inhibition in diabetic wound repair Wound Repair Regen 10 2002 295 301
42. S. Mangiafico, L.C. Costello-Boerrigter, I.A. Andersen, A. Cataliotti, and J.C. Burnett Jr. Neutral endopeptidase inhibition and the natriuretic peptide system: an evolving strategy in cardiovascular therapeutics Eur Heart J 34 2013 886 893c