CD19, a response regulator of B lymphocytes, regulates wound healing through hyaluronan-induced TLR4 signaling

American Journal of Pathology

Volumn 175, Issue 2, 2009, Pages 649-660

  Iwata, Yohei ^a,b   Yoshizaki, Ayumi ^a   Komura, Kazuhiro ^a   Shimizu, Kazuhiro ^a   Ogawa, Fumihide ^a   Hara, Toshihide ^a   Muroi, Eiji ^a   Bae, Sangjae ^a   Takenaka, Motoi ^a   Yukami, Toru ^c   Hasegawa, Minoru ^c   Fujimoto, Manabu ^c   Tomita, Yasushi ^b   Tedder, Thomas F ^d   Sato, Shinichi ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC FIBROBLAST GROWTH FACTOR; BASIC FIBROBLAST GROWTH FACTOR; CD19 ANTIGEN; GAMMA INTERFERON; HYALURONIC ACID; INTERLEUKIN 10; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; PLATELET DERIVED GROWTH FACTOR; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL INFILTRATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; GENE OVEREXPRESSION; MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN INJURY; WILD TYPE; WOUND HEALING; WOUND HEALING IMPAIRMENT;

EID: 68449102678     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080355     Document Type: Article

References (54)

1. Gillitzer R, Goebeler M: Chemokines in cutaneous wound healing. J Leukoc Biol 2001, 69:513-521
2. Hubner G, Brauchle M, Smola H, Madlener M, Fassler R, Werner S: Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine 1996, 8:548-556
3. Witte MB, Barbul A: General principles of wound healing. Surg Clin North Am 1997, 77:509-528
4. Martin P: Wound healing-aiming for perfect skin regeneration. Science 1997, 276:75-81
5. Singer AJ, Clark RA: Cutaneous wound healing. N Engl J Med 1999, 341:738-746
6. Park JE, Barbul A: Understanding the role of immune regulation in wound healing, Am J Surg 2004, 187:11S-16S
7. Blotnick S, Peoples GE, Freeman MR, Eberlein TJ, Klagsbrun M: T lymphocytes synthesize and export heparin-binding epidermal growth factor-like growth factor and basic fibroblast growth factor, mitogens for vascular cells and fibroblasts: differential production and release by CD4+ and CD8+ T cells. Proc Natl Acad Sci USA 1994, 91:2890-2894
8. Schaffer M, Barbul A: Lymphocyte function in wound healing and following injury. Br J Surg 1998, 85:444-460
9. Boyce DE, Jones WD, Ruge F, Harding KG, Moore K: The role of lymphocytes in human dermal wound healing. Br J Dermatol 2000, 143:59-65
10. Cowin AJ, Brosnan MP, Holmes TM, Ferguson MW: Endogenous inflammatory response to dermal wound healing in the fetal and adult mouse. Dev Dyn 1998, 212:385-393
11. Richards AM, Floyd DC, Terenghi G, McGrouther DA: Cellular changes in denervated tissue during wound healing in a rat model. Br J Dermatol 1999, 140:1093-1099
12. Lipsky PE: Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001, 2:764-766
13. Sato S, Hasegawa M, Fujimoto M, Tedder TF, Takehara K: Quantitative genetic variation in CD19 expression correlates with autoimmunity. J Immunol 2000, 165:6635-6643
14. Engel P, Zhou LJ, Ord DC, Sato S, Koller B, Tedder TF: Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 1995, 3:39-50
15. Sato S, Steeber DA, Jansen PJ, Tedder TF: CD19 expression levels regulate B lymphocyte development: human CD19 restores normal function in mice lacking endogenous CD19. J Immunol 1997, 158:4662-4669
16. Zhou LJ, Smith HM, Waldschmidt TJ, Schwarting R, Daley J, Tedder TF: Tissue-specific expression of the human CD19 gene in transgenic mice inhibits antigen-independent B-lymphocyte development. Mol Cell Biol 1994, 14:3884-3894
17. Subramaniam M, Saffaripour S, Van De Water L, Frenette PS, Mayadas TN, Hynes RO, Wagner DD: Role of endothelial selectins in wound repair. Am J Pathol 1997, 150:1701-1709
18. Meijerink J, Mandigers C, van de Locht L, Tonnissen E, Goodsaid F, Raemaekers J: A novel method to compensate for different amplification efficiencies between patient DNA samples in quantitative realtime PCR. J Mol Diagn 2001, 3:55-61
19. Metwali A, Blum AM, Elliott DE, Weinstock JV: IL-4 inhibits vasoactive intestinal peptide production by macrophages. Am J Physiol Gastrointest Liver Physiol 2002, 283:G115-G121
20. Arsenescu R, Blum AM, Metwali A, Elliott DE, Weinstock JV: IL-12 induction of mRNA encoding substance P in murine macrophages from the spleen and sites of inflammation. J Immunol 2005, 174:3906-3911
21. Marcelo CL, Kim YG, Kaine JL, Voorhees JJ: Stratification, specialization, and proliferation of primary keratinocyte cultures. Evidence of a functioning in vitro epidermal cell system. J Cell Biol 1978, 79:356-370
22. Mori T, Kawara S, Shinozaki M, Hayashi N, Kakinuma T, Igarashi A, Takigawa M, Nakanishi T, Takehara K: Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: a mouse fibrosis model. J Cell Physiol 1999, 181:153-159
23. Zhang Z, Schluesener HJ: Mammalian toll-like receptors: from endogenous ligands to tissue regeneration. Cell Mol Life Sci 2006, 63:2901-2907
24. Johnson GB, Brunn GJ, Platt JL: Cutting edge: an endogenous pathway to systemic inflammatory response syndrome (SIRS)-like reactions through Toll-like receptor 4. J Immunol 2004, 172:20-24
25. Taylor KR, Yamasaki K, Radek KA, Di Nardo A, Goodarzi H, Golenbock D, Beutler B, Gallo RL: Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J Biol Chem 2007, 282:18265-18275
26. Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, Ahrens T, Miyake K, Freudenberg M, Galanos C, Simon JC: Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002, 195:99-111
27. Taylor KR, Trowbridge JM, Rudisill JA, Termeer CC, Simon JC, Gallo RL: Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J Biol Chem 2004, 279:17079-17084
28. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, Homer RJ, Goldstein DR, Bucala R, Lee PJ, Medzhitov R, Noble PW: Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005, 11:1173-1179
29. Kodaira Y, Nair SK, Wrenshall LE, Gilboa E, Platt JL: Phenotypic and functional maturation of dendritic cells mediated by heparan sulfate. J Immunol 2000, 165:1599-1604
30. Johnson GB, Brunn GJ, Kodaira Y, Platt JL: Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol 2002, 168:5233-5239
31. Smiley ST, King JA, Hancock WW: Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 2001, 167:2887-2894
32. Werner S, Grose R: Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003, 83:835-870
33. Li X, Carter RH: Convergence of CD19 and B cell antigen receptor signals at MEK1 in the ERK2 activation cascade. J Immunol 1998, 161:5901-5908
34. Kawai T, Akira S: TLR signaling. Cell Death Differ 2006, 13:816-825
35. Price RD, Berry MG, Navsaria HA: Hyaluronic acid: the scientific and clinical evidence. J Plast Reconstr Aesthet Surg 2007, 60:1110-1119
36. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B: CD44 is the principal cell surface receptor for hyaluronate. Cell 1990, 61:1303-1313
37. Jiang D, Liang J, Noble PW: Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol 2007, 23:435-461
38. Macedo L, Pinhal-Enfield G, Alshits V, Elson G, Cronstein BN, Leibovich SJ: Wound healing is impaired in MyD88-deficient mice: a role for MyD88 in the regulation of wound healing by adenosine A2A receptors. Am J Pathol 2007, 171:1774-1788
39. Cohen-Sfady M, Nussbaum G, Pevsner-Fischer M, Mor F, Carmi P, Zanin-Zhorov A, Lider O, Cohen IR: Heat shock protein 60 activates B cells via the TLR4-MyD88 pathway. J Immunol 2005, 175:3594-3602
40. Barr TA, Brown S, Ryan G, Zhao J, Gray D: TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur J Immunol 2007, 37:3040-3053
41. Rafi A, Nagarkatti M, Nagarkatti PS: Hyaluronate-CD44 interactions can induce murine B-cell activation. Blood 1997, 89:2901-2908
42. Sato S, Ono N, Steeber DA, Pisetsky DS, Tedder TF: CD19 regulates B lymphocyte signaling thresholds critical for the development of B-1 lineage cells and autoimmunity. J Immunol 1996, 157:4371-4378
43. Yazawa N, Fujimoto M, Sato S, Miyake K, Asano N, Nagai Y, Takeuchi O, Takeda K, Okochi H, Akira S, Tedder TF, Tamaki K: CD19 regulates innate immunity by the toll-like receptor RP105 signaling in B lymphocytes. Blood 2003, 102:1374-1380
44. Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C: Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2, Proc Natl Acad Sci USA 1998, 95:5672-5677
45. Gallucci RM, Simeonova PP, Matheson JM, Kommineni C, Guriel JL, Sugawara T, Luster MI: Impaired cutaneous wound healing in interleukin-6-deficient and immunosuppressed mice. FASEB J 2000, 14:2525-2531
46. Lin ZQ, Kondo T, Ishida Y, Takayasu T, Mukaida N: Essential involvement of IL-6 in the skin wound-healing process as evidenced by delayed wound healing in IL-6-deficient mice. J Leukoc Biol 2003, 73:713-721
47. Mustoe TA, Pierce GF, Thomason A, Gramates P, Sporn MB, Deuel TF: Accelerated healing of incisional wounds in rats induced by transforming growth factor-beta. Science 1987, 237:1333-1336
48. Hebda PA: Stimulatory effects of transforming growth factor-beta and epidermal growth factor on epidermal cell outgrowth from porcine skin explant cultures. J Invest Dermatol 1988, 91:440-445
49. Pierce GF, Mustoe TA, Lingelbach J, Masakowski VR, Griffin GL, Senior RM, Deuel TF: Platelet-derived growth factor and transforming growth factor-beta enhance tissue repair activities by unique mechanisms. J Cell Biol 1989, 109:429-440
50. Pierce GF, Tarpley JE, Yanagihara D, Mustoe TA, Fox GM, Thomason A: Platelet-derived growth factor (BB homodimer), transforming growth factor-beta 1, and basic fibroblast growth factor in dermal wound healing. Neovessel and matrix formation and cessation of repair. Am J Pathol 1992, 140:1375-1388
51. Eming SA, Werner S, Bugnon P, Wickenhauser C, Siewe L, Utermohlen O, Davidson JM, Krieg T, Roers A: Accelerated wound closure in mice deficient for interleukin-10. Am J Pathol 2007, 170:188-202
52. Fujimoto M, Poe JC, Hasegawa M, Tedder TF: CD19 regulates intrinsic B lymphocyte signal transduction and activation through a novel mechanism of processive amplification. Immunol Res 2000, 22:281-298
53. Wang J, Watanabe T: Expression and function of Fas during differentiation and activation of B cells. Int Rev Immunol 1999, 18:367-379
54. Sato S, Fujimoto M, Hasegawa M, Takehara K: Altered blood B lymphocyte homeostasis in systemic sclerosis: expanded naive B cells and diminished but activated memory B cells. Arthritis Rheum 2004, 50:1918-1927