Resistin promotes angiogenesis in endothelial progenitor cells through inhibition of microRNA206: Potential implications for rheumatoid arthritis

Stem Cells

Volumn 33, Issue 7, 2015, Pages 2243-2255

  Su, Chen Ming ^a   Hsu, Chin Jung ^a,b   Tsai, Chun Hao ^a   Huang, Chun Yin ^a   Wang, Shih Wei ^c   Tang, Chih Hsin ^a,d,e  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c MACKAY MEDICAL COLLEGE   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e ASIA UNIVERSITY   (Taiwan)

Author keywords

Collagen induced arthritis; Endothelial progenitor cell; MicroRNA; Resistin; Rheumatoid arthritis

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MICRORNA; MICRORNA 206; PROTEIN KINASE C DELTA; RESISTIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN A;

3' UNTRANSLATED REGION; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HOMING; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN TARGETING; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYNOVIAL FLUID; SYNOVIUM; ADULT; ANIMAL; CHICK EMBRYO; FEMALE; GENETIC TRANSFECTION; GENETICS; METABOLISM; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

MUS;

ADULT; ANIMALS; ARTHRITIS, RHEUMATOID; CHICK EMBRYO; ENDOTHELIAL PROGENITOR CELLS; FEMALE; HUMANS; MALE; MICE; MICRORNAS; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; RESISTIN; TRANSFECTION;

EID: 84931564593     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2024     Document Type: Article

References (59)

1. Firestein GS,. Evolving concepts of rheumatoid arthritis. Nature 2003; 423: 356-361.
2. Szekanecz Z, Besenyei T, Szentpetery A, et al., Angiogenesis and vasculogenesis in rheumatoid arthritis. Curr Opin Rheumatol 2010; 22: 299-306.
3. Colville-Nash PR, Scott DL,. Angiogenesis and rheumatoid arthritis: Pathogenic and therapeutic implications. Ann Rheum Dis 1992; 51: 919-925.
4. Asahara T, Masuda H, Takahashi T, et al., Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999; 85: 221-228.
5. Yoder MC,. Human endothelial progenitor cells. Cold Spring Harb Perspect Med 2012; 2: a006692.
6. Jain RK, Carmeliet P,. SnapShot: Tumor angiogenesis. Cell 2012; 149: 1408-1408 e1401.
7. Urbich C, Dimmeler S,. Endothelial progenitor cells functional characterization. Trends Cardiovasc Med 2004; 14: 318-322.
8. Nolan DJ, Ciarrocchi A, Mellick AS, et al., Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. Genes Dev 2007; 21: 1546-1558.
9. Qatanani M, Szwergold NR, Greaves DR, et al., Macrophage-derived human resistin exacerbates adipose tissue inflammation and insulin resistance in mice. J Clin Invest 2009; 119: 531-539.
10. Reilly MP, Lehrke M, Wolfe ML, et al., Resistin is an inflammatory marker of atherosclerosis in humans. Circulation 2005; 111: 932-939.
11. Wen F, Yang Y, Jin D, et al., MiRNA-145 is involved in the development of resistin-induced insulin resistance in HepG2 cells. Biochem Biophys Res Commun 2014; 445: 517-523.
12. Luo Z, Zhang Y, Li F, et al., Resistin induces insulin resistance by both AMPK-dependent and AMPK-independent mechanisms in HepG2 cells. Endocrine 2009; 36: 60-69.
13. Cabou C, Vachoux C, Campistron G, et al., Brain GLP-1 signaling regulates femoral artery blood flow and insulin sensitivity through hypothalamic PKC-delta. Diabetes 2011; 60: 2245-2256.
14. Senolt L, Housa D, Vernerova Z, et al., Resistin in rheumatoid arthritis synovial tissue, synovial fluid and serum. Ann Rheum Dis 2007; 66: 458-463.
15. Filkova M, Haluzik M, Gay S, et al., The role of resistin as a regulator of inflammation: Implications for various human pathologies. Clin Immunol 2009; 133: 157-170.
16. Dessein PH, Norton GR, Woodiwiss AJ, et al., Independent relationship between circulating resistin concentrations and endothelial activation in rheumatoid arthritis. Ann Rheum Dis 2013; 72: 1586-1588.
17. Mu H, Ohashi R, Yan S, et al., Adipokine resistin promotes in vitro angiogenesis of human endothelial cells. Cardiovasc Res 2006; 70: 146-157.
18. Dang LT, Lawson ND, Fish JE,. MicroRNA control of vascular endothelial growth factor signaling output during vascular development. Arterioscler Thromb Vasc Biol 2013; 33: 193-200.
19. Suarez Y, Fernandez-Hernando C, Yu J, et al., Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA 2008; 105: 14082-14087.
20. Iborra M, Bernuzzi F, Invernizzi P, et al., MicroRNAs in autoimmunity and inflammatory bowel disease: Crucial regulators in immune response. Autoimmunity Rev 2012; 11: 305-314.
21. Seok JK, Lee SH, Kim MJ, et al., MicroRNA-382 induced by HIF-1alpha is an angiogenic miR targeting the tumor suppressor phosphatase and tensin homolog. Nucleic acids Res 2014; 42: 8062-8072.
22. Tang CH, Hsu CJ, Fong YC,. The CCL5/CCR5 axis promotes interleukin-6 production in human synovial fibroblasts. Arthritis Rheum 2010; 62: 3615-3624.
23. Wang HH, Lin CA, Lee CH, et al., Fluorescent gold nanoclusters as a biocompatible marker for in vitro and in vivo tracking of endothelial cells. ACS Nano 2011; 5: 4337-4344.
24. Wu MH, Huang CY, Lin JA, et al., Endothelin-1 promotes vascular endothelial growth factor-dependent angiogenesis in human chondrosarcoma cells. Oncogene 2014; 33: 1725-1735.
25. Wang HH, Su CH, Wu YJ, et al., Reduction of connexin43 in human endothelial progenitor cells impairs the angiogenic potential. Angiogenesis 2013; 16: 553-560.
26. Chung CH, Chang CH, Chen SS, et al., Butein inhibits angiogenesis of human endothelial progenitor cells via the translation dependent signaling pathway. Evid Based Complement Alternat Med 2013; 2013: 943187.
27. Backlund J, Li C, Jansson E, et al., C57BL/6 mice need MHC class II Aq to develop collagen-induced arthritis dependent on autoreactive T cells. Ann Rheum Dis 2013; 72: 1225-1232.
28. Huang CY, Chen SY, Tsai HC, et al., Thrombin induces epidermal growth factor receptor transactivation and CCL2 expression in human osteoblasts. Arthritis Rheum 2012; 64: 3344-3354.
29. Storgard C, Mikolon D, Stupack DG,. Angiogenesis assays in the chick CAM. Methods Mol Biol 2005; 294: 123-136.
30. Passaniti A, Taylor RM, Pili R, et al., A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Invest 1992; 67: 519-528.
31. Gomez R, Conde J, Scotece M, et al., What's new in our understanding of the role of adipokines in rheumatic diseases? Nat Rev Rheumatol 2011; 7: 528-536.
32. Bokarewa M, Nagaev I, Dahlberg L, et al., Resistin, an adipokine with potent proinflammatory properties. J Immunol 2005; 174: 5789-5795.
33. Silverman MD, Haas CS, Rad AM, et al., The role of vascular cell adhesion molecule 1/very late activation antigen 4 in endothelial progenitor cell recruitment to rheumatoid arthritis synovium. Arthritis Rheum 2007; 56: 1817-1826.
34. Bevaart L, Vervoordeldonk MJ, Tak PP,. Collagen-induced arthritis in mice. Methods Mol Biol 2010; 602: 181-192.
35. Pickens SR, Volin MV, Mandelin AM, 2nd et al. IL-17 contributes to angiogenesis in rheumatoid arthritis. J Immunol 2010; 184: 3233-3241.
36. Jamaluddin MS, Weakley SM, Yao Q, et al., Resistin: Functional roles and therapeutic considerations for cardiovascular disease. Br J Pharmacol 2012; 165: 622-632.
37. Park JY, Takahara N, Gabriele A, et al., Induction of endothelin-1 expression by glucose: An effect of protein kinase C activation. Diabetes 2000; 49: 1239-1248.
38. Lizotte F, Pare M, Denhez B, et al., PKCdelta impaired vessel formation and angiogenic factor expression in diabetic ischemic limbs. Diabetes 2013; 62: 2948-2957.
39. Turrell HE, Rodrigo GC, Norman RI, et al., Phenylephrine preconditioning involves modulation of cardiac sarcolemmal K(ATP) current by PKC delta, AMPK and p38 MAPK. J Mol Cell Cardiol 2011; 51: 370-380.
40. Singh RP, Massachi I, Manickavel S, et al., The role of miRNA in inflammation and autoimmunity. Autoimmunity Rev 2013; 12: 1160-1165.
41. Rall LC, Roubenoff R,. Rheumatoid cachexia: Metabolic abnormalities, mechanisms and interventions. Rheumatology 2004; 43: 1219-1223.
42. Silswal N, Singh AK, Aruna B, et al., Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NF-kappaB-dependent pathway. Biochem Biophys Res Commun 2005; 334: 1092-1101.
43. Pang SS, Le YY,. Role of resistin in inflammation and inflammation-related diseases. Cell Mol Immunol 2006; 3: 29-34.
44. Tysome JR, Lemoine NR, Wang Y,. Combination of anti-angiogenic therapy and virotherapy: Arming oncolytic viruses with anti-angiogenic genes. Curr Opin Mol Ther 2009; 11: 664-669.
45. Ozgonenel L, Cetin E, Tutun S, et al., The relation of serum vascular endothelial growth factor level with disease duration and activity in patients with rheumatoid arthritis. Clin Rheumatol 2010; 29: 473-477.
46. Westerweel PE, Verhaar MC,. Endothelial progenitor cell dysfunction in rheumatic disease. Nat Rev Rheum 2009; 5: 332-340.
47. Hemmerle T, Doll F, Neri D,. Antibody-based delivery of IL4 to the neovasculature cures mice with arthritis. Proc Natl Acad Sci USA 2014; 111: 12008-12012.
48. Amin MA, Campbell PL, Ruth JH, et al., A key role for Fut1-regulated angiogenesis and ICAM-1 expression in K/BxN arthritis. Ann Rheum Dis 2014 [Epub ahead of print].
49. Brand DD, Kang AH, Rosloniec EF,. Immunopathogenesis of collagen arthritis. Springer Semin Immunopathol 2003; 25: 3-18.
50. Lorenzi O, Frieden M, Villemin P, et al., Protein kinase C-delta mediates von Willebrand factor secretion from endothelial cells in response to vascular endothelial growth factor (VEGF) but not histamine. J Thromb Haemost 2008; 6: 1962-1969.
51. Holmes K, Chapman E, See V, et al., VEGF stimulates RCAN1.4 expression in endothelial cells via a pathway requiring Ca2+/calcineurin and protein kinase C-delta. PloS One 2010; 5: e11435.
52. Berk BC, Taubman MB, Cragoe EJ, Jr,. et al. Thrombin signal transduction mechanisms in rat vascular smooth muscle cells. Calcium and protein kinase C-dependent and -independent pathways. J Biol Chem 1990; 265: 17334-17340.
53. Gliki G, Wheeler-Jones C, Zachary I,. Vascular endothelial growth factor induces protein kinase C (PKC)-dependent Akt/PKB activation and phosphatidylinositol 3'-kinase-mediates PKC delta phosphorylation: Role of PKC in angiogenesis. Cell Biol Int 2002; 26: 751-759.
54. He L, Hannon GJ,. MicroRNAs: Small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5: 522-531.
55. Landskroner-Eiger S, Moneke I, Sessa WC,. miRNAs as modulators of angiogenesis. Cold Spring Harbor Perspect Med 2013; 3: a006643.
56. Esquela-Kerscher A, Slack FJ,. Oncomirs-MicroRNAs with a role in cancer. Nat Rev Cancer 2006; 6: 259-269.
57. Zhong D, Huang G, Zhang Y, et al., MicroRNA-1 and microRNA-206 suppress LXRalpha-induced lipogenesis in hepatocytes. Cell Signal 2013; 25: 1429-1437.
58. Chen X, Yan Q, Li S, et al., Expression of the tumor suppressor miR-206 is associated with cellular proliferative inhibition and impairs invasion in ERalpha-positive endometrioid adenocarcinoma. Cancer Lett 2012; 314: 41-53.
59. Stahlhut C, Suarez Y, Lu J, et al., miR-1 and miR-206 regulate angiogenesis by modulating VegfA expression in zebrafish. Development. 2012; 139: 4356-4364.