Lymphatic endothelial cells efferent to inflamed joints produce iNOS and inhibit lymphatic vessel contraction and drainage in TNF-induced arthritis in mice

Arthritis Research and Therapy

Volumn 18, Issue 1, 2016, Pages

  Liang, Qianqian ^a,b   Ju, Yawen ^b   Chen, Yan ^a   Wang, Wensheng ^b   Li, Jinlong ^a   Zhang, Li ^a   Xu, Hao ^a,b   Wood, Ronald W ^b   Schwarz, Edward M ^b   Boyce, Brendan F ^b   Wang, Yongjun ^a   Xing, Lianping ^b  

^a SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Ferulic acid; Inducible nitric oxide synthase (iNOS); Lymphatic endothelial cells (LECs); Lymphatic function; Lymphatic smooth muscle cells (LSMC); Rheumatoid arthritis; TNF

Indexed keywords

FERULIC ACID; INDUCIBLE NITRIC OXIDE SYNTHASE; N6 (1 IMINOETHYL)LYSINE; PODOPLANIN; TUMOR NECROSIS FACTOR; COUMARIC ACID; NOS2 PROTEIN, MOUSE; SCAVENGER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; BONE EROSION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME SYNTHESIS; FEMALE; GENE EXPRESSION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LYMPH VESSEL; MALE; MOUSE; NEAR INFRARED SPECTROSCOPY; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; EXPERIMENTAL ARTHRITIS; FLOW CYTOMETRY; INFLAMMATION; METABOLISM; MUSCLE CONTRACTION; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; SMOOTH MUSCLE; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; BLOTTING, WESTERN; COUMARIC ACIDS; ENDOTHELIAL CELLS; FLOW CYTOMETRY; FREE RADICAL SCAVENGERS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LYMPHATIC VESSELS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE CONTRACTION; MUSCLE, SMOOTH; NITRIC OXIDE SYNTHASE TYPE II; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84960358914     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-016-0963-8     Document Type: Article

References (56)

1. Zawieja D. Lymphatic biology and the microcirculation: past, present and future. Microcirculation. 2005;12(1):141-50.
2. Wilting J, Becker J, Buttler K, Weich HA. Lymphatics and inflammation. Curr Med Chem. 2009;16(34):4581-92.
3. Olszewski WL, Pazdur J, Kubasiewicz E, Zaleska M, Cooke CJ, Miller NE. Lymph draining from foot joints in rheumatoid arthritis provides insight into local cytokine and chemokine production and transport to lymph nodes. Arthritis Rheum. 2001;44(3):541-9.
4. Wauke K, Nagashima M, Ishiwata T, Asano G, Yoshino S. Expression and localization of vascular endothelial growth factor-C in rheumatoid arthritis synovial tissue. J Rheumatol. 2002;29(1):34-8.
5. Zhang Q, Lu Y, Proulx ST, Guo R, Yao Z, Schwarz EM, et al. Increased lymphangiogenesis in joints of mice with inflammatory arthritis. Arthritis Res Ther. 2007;9(6):R118.
6. Polzer K, Baeten D, Soleiman A, Distler J, Gerlag DM, Tak PP, et al. Tumour necrosis factor blockade increases lymphangiogenesis in murine and human arthritic joints. Ann Rheum Dis. 2008;67(11):1610-6.
7. Proulx ST, Kwok E, You Z, Beck CA, Shealy DJ, Ritchlin CT, et al. MRI and quantification of draining lymph node function in inflammatory arthritis. Ann N Y Acad Sci. 2007;1117:106-23.
8. hi B cells in inflamed lymph nodes are associated with the onset of inflammatory-erosive arthritis in TNF-transgenic mice and are targets of anti-CD20 therapy. J Immunol. 2010;184(11):6142-50.
9. Benaglio F, Vitolo B, Scarabelli M, Binda E, Bugatti S, Caporali R, et al. The draining lymph node in rheumatoid arthritis: current concepts and research perspectives. Biomed Res Int. 2015;2015:420251.
10. Keffer J, Probert L, Cazlaris H, Georgopoulos S, Kaslaris E, Kioussis D, et al. Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J. 1991;10(13):4025-31.
11. Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell. 1996;87(5):811-22.
12. Bouta EM, Li J, Ju Y, Brown EB, Ritchlin CT, Xing L, et al. The role of the lymphatic system in inflammatory-erosive arthritis. Semin Cell Dev Biol. 2015;38:90-7.
13. Zhou Q, Wood R, Schwarz EM, Wang YJ, Xing L. Near-infrared lymphatic imaging demonstrates the dynamics of lymph flow and lymphangiogenesis during the acute versus chronic phases of arthritis in mice. Arthritis Rheum. 2010;62(7):1881-9.
14. Li J, Ju Y, Bouta EM, Xing L, Wood RW, Kuzin I, et al. Efficacy of B cell depletion therapy for murine joint arthritis flare is associated with increased lymphatic flow. Arthritis Rheum. 2013;65(1):130-8.
15. Bouta EM, Wood RW, Perry SW, Brown EB, Ritchlin CT, Xing L, et al. Measuring intranodal pressure and lymph viscosity to elucidate mechanisms of arthritic flare and therapeutic outcomes. Ann N Y Acad Sci. 2011;1240:47-52.
16. van der Flier A, Badu-Nkansah K, Whittaker CA, Crowley D, Bronson RT, Lacy-Hulbert A, et al. Endothelial α5 and αv integrins cooperate in remodeling of the vasculature during development. Development. 2010;137(14):2439-49.
17. Zhou F, Chang Z, Zhang L, Hong YK, Shen B, Wang B, et al. Akt/protein kinase B is required for lymphatic network formation, remodeling, and valve development. Am J Pathol. 2010;177(4):2124-33.
18. von der Weid PY, Zawieja DC. Lymphatic smooth muscle: the motor unit of lymph drainage. Int J Biochem Cell Biol. 2004;36(7):1147-53.
19. Van Helden DF. Pacemaker potentials in lymphatic smooth muscle of the guinea-pig mesentery. J Physiol. 1993;471:465-79.
20. ATP channel pathway in the mesenteric lymphatic pump dysfunction observed in the guinea pig model of TNBS-induced ileitis. Am J Physiol Gastrointest Liver Physiol. 2013;304(6):G623-34.
21. Schmid-Schonbein GW. Nitric oxide (NO) side of lymphatic flow and immune surveillance. Proc Natl Acad Sci U S A. 2012;109(1):3-4.
22. Liao S, Cheng G, Conner DA, Huang Y, Kucherlapati RS, Munn LL, et al. Impaired lymphatic contraction associated with immunosuppression. Proc Natl Acad Sci U S A. 2011;108(46):18784-9.
23. Scallan JP, Davis MJ. Genetic removal of basal nitric oxide enhances contractile activity in isolated murine collecting lymphatic vessels. J Physiol. 2013;591(Pt 8):2139-56.
24. Farrell AJ, Blake DR, Palmer RM, Moncada S. Increased concentrations of nitrite in synovial fluid and serum samples suggest increased nitric oxide synthesis in rheumatic diseases. Ann Rheum Dis. 1992;51(11):1219-22.
25. Grabowski PS, England AJ, Dykhuizen R, Copland M, Benjamin N, Reid DM, et al. Elevated nitric oxide production in rheumatoid arthritis: detection using the fasting urinary nitrate:creatinine ratio. Arthritis Rheum. 1996;39(4):643-7.
26. McInnes IB, Leung BP, Field M, Wei XQ, Huang FP, Sturrock RD, et al. Production of nitric oxide in the synovial membrane of rheumatoid and osteoarthritis patients. J Exp Med. 1996;184(4):1519-24.
27. Sakurai H, Kohsaka H, Liu MF, Higashiyama H, Hirata Y, Kanno K, et al. Nitric oxide production and inducible nitric oxide synthase expression in inflammatory arthritides. J Clin Invest. 1995;96(5):2357-63.
28. Connor JR, Manning PT, Settle SL, Moore WM, Jerome GM, Webber RK, et al. Suppression of adjuvant-induced arthritis by selective inhibition of inducible nitric oxide synthase. Eur J Pharmacol. 1995;273(1-2):15-24.
29. Grabowski PS, Wright PK, Van 't Hof RJ, Helfrich MH, Ohshima H, Ralston SH. Immunolocalization of inducible nitric oxide synthase in synovium and cartilage in rheumatoid arthritis and osteoarthritis. Br J Rheumatol. 1997;36(6):651-5.
30. Leak LV, Cadet JL, Griffin CP, Richardson K. Nitric oxide production by lymphatic endothelial cells in vitro. Biochem Biophys Res Commun. 1995;217(1):96-105.
31. McCartney-Francis N, Allen JB, Mizel DE, Albina JE, Xie QW, Nathan CF, et al. Suppression of arthritis by an inhibitor of nitric oxide synthase. J Exp Med. 1993;178(2):749-54.
32. Ribera J, Pauta M, Melgar-Lesmes P, Tugues S, Fernández-Varo G, Held KF, et al. Increased nitric oxide production in lymphatic endothelial cells causes impairment of lymphatic drainage in cirrhotic rats. Gut. 2013;62(1):138-45.
33. Yang CL, Or TC, Ho MH, Lau AS. Scientific basis of botanical medicine as alternative remedies for rheumatoid arthritis. Clin Rev Allergy Immunol. 2013;44(3):284-300.
34. Lee WY, Chen HY, Chen KC, Chen CY. Treatment of rheumatoid arthritis with traditional Chinese medicine. Biomed Res Int. 2014;2014:528018.
35. Guo R, Zhou Q, Proulx ST, Wood R, Ji RC, Ritchlin CT, et al. Inhibition of lymphangiogenesis and lymphatic drainage via vascular endothelial growth factor receptor 3 blockade increases the severity of inflammation in a mouse model of chronic inflammatory arthritis. Arthritis Rheum. 2009;60(9):2666-76.
36. high osteoclast precursors in tumor necrosis factor α-transgenic mice. Arthritis Rheum. 2004;50(1):265-76.
37. Proulx ST, Kwok E, Beck CA, Shealy DJ, Ritchlin CT, Award H, et al.Longitudinal assessment of synovial, lymph node, and bone volumes in inflammatory arthritis in mice using in vivo MRI and micro-CT. Arthritis Rheum. 2007;56(12):4024-37.
38. Yu Y, Fan SM, Yuan SJ, Tashiro S, Onodera S, Ikejima T. Nitric oxide (NO) generation but not ROS plays a major role in silibinin-induced autophagic and apoptotic death in human epidermoid carcinoma A431 cells. Free Radic Res. 2012;46(11):1346-60.
39. Muthuchamy M, Gashev A, Boswell N, Dawson N, Zawieja D. Molecular and functional analyses of the contractile apparatus in lymphatic muscle. FASEB J. 2003;17(8):920-2.
40. Sironi M, Conti A, Bernasconi S, Fra AM, Pasqualini F, Nebuloni M, et al. Generation and characterization of a mouse lymphatic endothelial cell line. Cell Tissue Res. 2006;325(1):91-100.
41. hi B cell translocation and ipsilateral lymph node collapse is associated with asymmetric arthritic flare in TNF-Tg mice. Arthritis Res Ther. 2011;13(4):R138.
42. Zhang P, Li J, Han Y, Yu XW, Qin L. Traditional Chinese medicine in the treatment of rheumatoid arthritis: a general review. Rheumatol Int. 2010;30(6):713-8.
43. Zhao XX, Peng C, Zhang H, Qin LP. Sinomenium acutum: a review of chemistry, pharmacology, pharmacokinetics, and clinical use. Pharm Biol. 2012;50(8):1053-61.
44. Ramgolam V, Ang SG, Lai YH, Loh CS, Yap HK. Traditional Chinese medicines as immunosuppressive agents. Ann Acad Med Singapore. 2000;29(1):11-6.
45. Ho LJ, Lai JH. Chinese herbs as immunomodulators and potential disease-modifying antirheumatic drugs in autoimmune disorders. Curr Drug Metab. 2004;5(2):181-92.
46. Wang T, Wei Z, Dou Y, Yang Y, Leng D, Kong L, et al. Intestinal interleukin-10 mobilization as a contributor to the anti-arthritis effect of orally administered madecassoside: a unique action mode of saponin compounds with poor bioavailability. Biochem Pharmacol. 2015;94(1):30-8.
47. Yao H, Shi P, Shao Q, Fan X. Chemical fingerprinting and quantitative analysis of a Panax notoginseng preparation using HPLC-UV and HPLC-MS. Chin Med. 2011;6:9.
48. Ye HZ, Zheng CS, Xu XJ, Wu MX, Liu XX. Potential synergistic and multitarget effect of herbal pair Chuanxiong Rhizome-Paeonia Albifora Pall on osteoarthritis disease: a computational pharmacology approach. Chin J Integr Med. 2011;17(9):698-703.
49. 2 levels. Arthritis Res Ther. 2007;9(4):R64.
50. Firestein GS. The disease formerly known as rheumatoid arthritis. Arthritis Res Ther. 2014;16(3):114.
51. Zhou Q, Guo R, Wood R, Boyce BF, Liang Q, Wang YJ, et al. Vascular endothelial growth factor C attenuates joint damage in chronic inflammatory arthritis by accelerating local lymphatic drainage in mice. Arthritis Rheum. 2011;63(8):2318-28.
52. Yao Z, Xing L, Boyce BF. NF-ΚB p100 limits TNF-induced bone resorption in mice by a TRAF3-dependent mechanism. J Clin Investig. 2009;119(10):3024-34.
53. Vermeire K, Thielemans L, Matthys P, Billiau A. The effects of NO synthase inhibitors on murine collagen-induced arthritis do not support a role of NO in the protective effect of IFN-γ. J Leukoc Biol. 2000;68(1):119-24.
54. Cuzzocrea S, Chatterjee PK, Mazzon E, McDonald MC, Dugo L, Di Paola R, et al. Beneficial effects of GW274150, a novel, potent and selective inhibitor of iNOS activity, in a rodent model of collagen-induced arthritis. Eur J Pharmacol. 2002;453(1):119-29.
55. Seymour M, Petavy F, Chiesa F, Perry H, Lukey PT, Binks M, et al. Ultrasonographic measures of synovitis in an early phase clinical trial: a double-blind, randomised, placebo and comparator controlled phase IIa trial of GW274150 (a selective inducible nitric oxide synthase inhibitor) in rheumatoid arthritis. Clin Exp Rheumatol. 2012;30(2):254-61.
56. Tisljar M, Grabarević Z, Artuković B, Dzaja P, Cenan S, Zelenika TA, et al. The impact of l-NAME and l-arginine chronic toxicity induced lesions on ascites-pulmonary hypertension syndrome development in broiler chickens. Coll Antropol. 2011;35(2):547-56.