Galectin-1 accelerates wound healing by regulating the neuropilin-1/Smad3/NOX4 pathway and ROS production in myofibroblasts

Journal of Investigative Dermatology

Volumn 135, Issue 1, 2015, Pages 258-268

  Lin, Yueh Te ^a   Chen, Jhih Sian ^a   Wu, Ming Heng ^b   Hsieh, I Shan ^a   Liang, Chen Hsien ^a   Hsu, Cheng Lung ^c   Hong, Tse Ming ^a   Chen, Yuh Ling ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; FIBRONECTIN; GALECTIN 1; GLUCOSE; NEUROPILIN 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMAD3 PROTEIN; LGALS1 PROTEIN, HUMAN; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMAD3 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FIBROBLAST; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; SCAR FORMATION; SIGNAL TRANSDUCTION; SKIN INJURY; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UPREGULATION; WESTERN BLOTTING; WOUND CLOSURE; WOUND HEALING; WOUND HEALING IMPAIRMENT; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GENETICS; GINGIVA; HEK293 CELL LINE; INJURIES; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SKIN;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; FIBROBLASTS; GALECTIN 1; GINGIVA; HEK293 CELLS; HUMANS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; NEUROPILIN-1; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SKIN; SMAD3 PROTEIN; WOUND HEALING;

EID: 84925227618     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.288     Document Type: Article

References (54)

1. Al-Salam S, Hashmi S (2014) Galectin-1 in early acute myocardial infarction. PLoS One 9:e8699
2. Almkvist J, Dahlgren C, Leffler H et al. (2002) Activation of the neutrophil nicotinamide adenine dinucleotide phosphate oxidase by galectin-1. J Immunol 168:4034-41
3. Amara N, Goven D, Prost F et al. (2010) NOX4/NADPH oxidase expression is increased in pulmonary fibroblasts from patients with idiopathic pulmonary fibrosis and mediates TGFbeta1-induced fibroblast differentiation into myofibroblasts. Thorax 65:733-8
4. auf dem Keller U, Kümin A, Braun S et al. (2006) Reactive oxygen species and their detoxification in healing skin wounds. J Investig Dermatol Symp Proc 11:106-11
5. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313
6. Bondi CD, Manickam N, Lee DY et al. (2010) NAD(P)H oxidase mediates TGF-beta1-induced activation of kidney myofibroblasts. J Am Soc Nephrol 21:93-102
7. Bryan N, Ahswin H, Smart N et al. (2012) Reactive oxygen species (ROS)-a family of fate deciding molecules pivotal in constructive inflammation and wound healing. Eur Cell Mater 24:249-65
8. Cao S, Yaqoob U, Das A et al. (2010a) Neuropilin-1 promotes cirrhosis of the rodent and human liver by enhancing PDGF/TGF-beta signaling in hepatic stellate cells. J Clin Invest 120:2379-94
9. Cao Y, Szabolcs A, Dutta SK et al. (2010b) Neuropilin-1 mediates divergent R-Smad signaling and the myofibroblast phenotype. J Biol Chem 285: 31840-8
10. Cao Z, SaidN, Amin S et al. (2002) Galectins-3 and-7, but not galectin-1, play a role in re-epithelialization of wounds. J Biol Chem 277:42299-305
11. Chen HY, Lo CH, Li CS et al. (2012) Galectins and cutaneous immunity. Dermatol Sinica 30:121-7
12. Clark RA (2008) Oxidative stress and ''senescent'' fibroblasts in non-healing wounds as potential therapeutic targets. J Invest Dermatol 128:2361-4
13. Clark RA, Ghosh K, Tonnesen MG (2007) Tissue engineering for cutaneous wounds. J Invest Dermatol 127:1018-29
14. Cucoranu I, Clempus R, Dikalova A et al. (2005) NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 97:900-7
15. Darby I, Skalli O, Gabbiani G (1990) Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 63:21-9
16. Diegelmann RF, Evans MC (2004) Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci 9:283-9
17. Dvoránková B, Szabo P, Lacina L et al. (2011) Human galectins induce conversion of dermal fibroblasts into myofibroblasts and production of extracellular matrix: potential application in tissue engineering and wound repair. Cells Tissues Organs 194:469-80
18. Fitzner B, Walzel H, Sparmann G et al. (2005) Galectin-1 is an inductor of pancreatic stellate cell activation. Cell Signal 17:1240-7
19. Gál P, Vasilenko T, Kostelnikova M et al. (2011) Open wound healing in vivo: monitoring binding and presence of adhesion/growth-regulatory galectins in rat skin during the course of complete re-epithelialization. Acta Histochem Cytochem 44:191-9
20. Goldring K, Jones GE, Thiagarajah R et al. (2002) The effect of galectin-1 on the differentiation of fibroblasts and myoblasts in vitro. J Cell Sci 115: 355-66
21. Graves DT, Liu R, Alikhani M et al. (2006) Diabetes-enhanced inflammation and apoptosis-impact on periodontal pathology. J Dent Res 85:15-21
22. Grendel T, Sokolsky J, Vascakova A et al. (2012) Early stages of trachea healing process: (immuno/lectin) histochemical monitoring of selected markers and adhesion/growth-regulatory endogenous lectins. Folia Biol (Praha) 58:135-43
23. Guo S, Dipietro LA (2010) Factors affecting wound healing. J Dent Res 89:219-29
24. Harding KG, Moore K, Phillips TJ (2005) Wound chronicity and fibroblast senescence-implications for treatment. Int Wound J 2:364-8
25. Hecker L, Vittal R, Jones T et al. (2009) NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat Med 15:1077-81
26. Hsieh SH, Ying NW, Wu MH et al. (2008) Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene 27:3746-53
27. Huo Y, Qiu WY, Pan Q et al. (2009) Reactive oxygen species (ROS) are essential mediators in epidermal growth factor (EGF)-stimulated corneal epithelial cell proliferation, adhesion, migration, and wound healing. Exp Eye Res 89:876-86
28. Kaltalioglu K, Coskun-Cevher S, Tugcu-Demiroz F et al. (2013) PDGF supplementation alters oxidative events in wound healing process: a time course study. Arch Dermatol Res 305:415-22
29. Kĺma J, Lacina L, Dvorankova B et al. (2009) Differential regulation of galectin expression/reactivity during wound healing in porcine skin and in cultures of epidermal cells with functional impact on migration. Physiol Res 58:873-84
30. Lai A, Hosseini-Tabatabaei A, Hartwell R et al. (2013) Topical application of aminopeptidase N-neutralizing antibody accelerates wound closure. Mol Cell Biochem 372:95-100
31. Lerman OZ, Galiano RD, Armour M et al. (2003) Cellular dysfunction in the diabetic fibroblast: impairment in migration, vascular endothelial growth factor production, and response to hypoxia. Am J Pathol 162:303-12
32. Loots MA, Lamme EN, Mekkes JR et al. (1999) Cultured fibroblasts from chronic diabetic wounds on the lower extremity (non-insulin-dependent diabetes mellitus) show disturbed proliferation. Arch Dermatol Res 291:93-9
33. Maeda N, Kawada N, Seki S et al. (2003) Stimulation of proliferation of rat hepatic stellate cells by galectin-1 and galectin-3 through different intracellular signaling pathways. J Biol Chem 278:18938-44
34. Maeda N, Kawada N, Seki S et al. (2004) Involvement of Galectin-1 and Galectin-3 in proliferation and migration of rat hepatic stellate cells in culture. Comp Hepatol 3:S10
35. Masamune A, Satoh M, Hirabayashi J et al. (2006) Galectin-1 induces chemokine production and proliferation in pancreatic stellate cells. Am J Physiol Gastrointest Liver Physiol 290:G729-36
36. Menke NB, Ward KR, Witten TM et al. (2007) Impaired wound healing. Clin Dermatol 25:19-25
37. Poirier F, Robertson EJ (1993) Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development 119:1229-36
38. Prud'homme GJ, Glinka Y (2012) Neuropilins are multifunctional coreceptors involved in tumor initiation, growth, metastasis and immunity. Oncotarget 3:921-39
39. Rossini AA, Like AA, Chick WL et al. (1977) Studies of streptozotocin-induced insulitis and diabetes. Proc Natl Acad Sci USA 74:2485-9
40. Sakaguchi M, Arruda-Carvalho M, Kang NH et al. (2011) Impaired spatial and contextual memory formation in galectin-1 deficient mice. Mol Brain 4:33
41. Salatino M, Croci DO, Bianco GA et al. (2008) Galectin-1 as a potential therapeutic target in autoimmune disorders and cancer. Expert Opin Biol Ther 8:45-57
42. Sampson N, Berger P, Zenzmaier C (2012) Therapeutic targeting of redox signaling in myofibroblast differentiation and age-related fibrotic disease. Oxid Med Cell Longev 2012:45827
43. Sampson N, Koziel R, Zenzmaier C et al. (2011) ROS signaling by NOX4 drives fibroblast-to-myofibroblast differentiation in the diseased prostatic stroma. Mol Endocrinol 25:503-15
44. Sarrazy V, Billet F, Micallef L et al. (2011) Mechanisms of pathological scarring: role of myofibroblasts and current developments. Wound Repair Regen 19:s10-5
45. Seropian IM, Cerliani JP, Toldo S et al. (2013) Galectin-1 controls cardiac inflammation and ventricular remodeling during acute myocardial infarction. Am J Pathol 182:29-40
46. Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341: 738-46
47. Smetana K Jr, André S, Kaltner H et al. (2013) Context-dependent multifunctionality of galectin-1: a challenge for defining the lectin as therapeutic target. Expert Opin Ther Targets 17:379-92
48. Thijssen VL, Postel R, Brandwijk RJ et al. (2006) Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci USA 103:15975-80
49. Tomasek JJ, Gabbiani G, Hinz B et al. (2002) Myofibroblasts and mechanoregulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349-63
50. Velnar T, Bailey T, Smrkolj V (2009) The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res 37:1528-42
51. Welt K, Hinrichs R, Weiss JM et al. (2009) Skin diseases in Europe. Wound healing. Eur J Dermatol 19:413-6
52. Wu MH, Hong HC, Hong TM et al. (2011) Targeting galectin-1 in carcinomaassociated fibroblasts inhibits oral squamous cell carcinoma metastasis by downregulating MCP-1/CCL2 expression. Clin Cancer Res 17:1306-16
53. Wu MH, Hong TM, Cheng HW et al. (2009) Galectin-1-mediated tumor invasion and metastasis, up-regulated matrix metalloproteinase expression, and reorganized actin cytoskeletons. Mol Cancer Res 7:311-8
54. Xue X, Lu Z, Tang D et al. (2011) Galectin-1 secreted by activated stellate cells in pancreatic ductal adenocarcinoma stroma promotes proliferation and invasion of pancreatic cancer cells: an in vitro study on the microenvironment of pancreatic ductal adenocarcinoma. Pancreas 40:832-9