The role of pericyte detachment in vascular rarefaction

Journal of Vascular Research

Volumn 51, Issue 4, 2014, Pages 247-258

  Schrimpf, Claudia ^a   Teebken, Omke E ^a   Wilhelmi, Mathias ^a   Duffield, Jeremy S ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelial cells; Fibrosis; Microcirculation; Pericyte endothelial interaction; Pericytes

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; METALLOPROTEINASE; PLATELET DERIVED GROWTH FACTOR B; VASCULOTROPIN A; WNT PROTEIN;

BLOOD VESSEL WALL; CELL FUNCTION; CELL INTERACTION; ENDOTHELIUM CELL; FIBROSING ALVEOLITIS; HUMAN; KIDNEY DISEASE; NONHUMAN; PERICYTE; REVIEW; WNT SIGNALING PATHWAY; CAPILLARY; CELL COMMUNICATION; CYTOLOGY; FIBROSIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SCAR; VASCULAR DISEASE;

CAPILLARIES; CELL COMMUNICATION; CICATRIX; ENDOTHELIAL CELLS; FIBROSIS; HUMANS; PERICYTES; VASCULAR DISEASES;

EID: 84908894844     PISSN: 10181172     EISSN: 14230135     Source Type: Journal    
DOI: 10.1159/000365149     Document Type: Review

References (122)

1. Roberts IS, Burrows C, Shanks JH, Venning M, McWilliam LJ: Interstitial myofibroblasts: predictors of progression in membranous nephropathy. J Clin Pathol 1997; 50: 123-127.
2. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB: Myofibroblasts. 1. Paracrine cells important in health and disease. Am J Physiol 1999; 277:C1-C9.
3. Badid C, Desmouliere A, Babici D, Hadj-Aissa A, McGregor B, Lefrancois N, Touraine JL, Laville M: Interstitial expression of alpha- SMA: an early marker of chronic renal allograft dysfunction. Nephrol Dial Transplant 2002; 17: 1993-1998.
4. Kang DH, Kanellis J, Hugo C, Truong L, Anderson S, Kerjaschki D, Schreiner GF, Johnson RJ: Role of the microvascular endothelium in progressive renal disease. J Am Soc Nephrol 2002; 13: 806-816.
5. Siao CJ, Lorentz CU, Kermani P, Marinic T, Carter J, McGrath K, Padow VA, Mark W, Falcone DJ, Cohen-Gould L, Parrish DC, Habecker BA, Nykjaer A, Ellenson LH, Tessarollo L, Hempstead BL: ProNGF, a cytokine induced after myocardial infarction in humans, targets pericytes to promote microvascular damage and activation. J Exp Med 2012; 209: 2291-2305.
6. Hung C, Linn G, Chow YH, Kobayashi A, Mittelsteadt K, Altemeier WA, Gharib SA, Schnapp LM, Duffield JS: Role of lung pericytes and resident fibroblasts in the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 2013; 188: 820-830.
7. Bachem MG, Zhou Z, Zhou S, Siech M: Role of stellate cells in pancreatic fibrogenesis associated with acute and chronic pancreatitis. J Gastroenterol Hepatol 2006; 21(suppl 3):S92- S96.
8. Friedman SL, Sheppard D, Duffield JS, Violette S: Therapy for fibrotic diseases: nearing the starting line. Sci Transl Med 2013; 5: 167sr161.
9. Goritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisen J: A pericyte origin of spinal cord scar tissue. Science 2011; 333: 238-242.
10. Libby P, Ridker PM, Hansson GK: Progress and challenges in translating the biology of atherosclerosis. Nature 2011; 473: 317-325.
11. Kisseleva T, Cong M, Paik Y, Scholten D, Jiang C, Benner C, Iwaisako K, Moore-Morris T, Scott B, Tsukamoto H, Evans SM, Dillmann W, Glass CK, Brenner DA: Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc Natl Acad Sci USA 2012; 109: 9448-9453.
12. Dulauroy S, Di Carlo SE, Langa F, Eberl G, Peduto L: Lineage tracing and genetic ablation of ADAM12(+) perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nat Med 2012; 18: 1262- 1270.
13. Natarajan A, Lemos DR, Rossi FM: Fibro/adipogenic progenitors: a double-edged sword in skeletal muscle regeneration. Cell Cycle 2010; 9: 2045-2046.
14. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS: Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 2011; 176: 85-97.
15. Lin SL, Kisseleva T, Brenner DA, Duffield JS: Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 2008; 173: 1617-1627.
16. Duffield J: Cellular and molecular mechanisms in kidney fibrosis. J Clin Invest 2014; 124: 2299-2306.
17. LeBleu VS, Taduri G, O'Connell J, Teng Y, Cooke VG, Woda C, Sugimoto H, Kalluri R: Origin and function of myofibroblasts in kidney fibrosis. Nat Med 2013; 19: 1047-1053.
18. Schrimpf C, Duffield JS: Mechanisms of fibrosis: the role of the pericyte. Curr Opin Nephrol Hypertens 2011; 20: 297-305.
19. Hung C, Linn G, Chow YH, Kobayashi A, Mittelsteadt K, Altemeier WA, Gharib SA, Schnapp LM, Duffield JS: Role of lung pericytes and resident fibroblasts in the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 2013; 188: 820-830.
20. Benjamin LE, Golijanin D, Itin A, Pode D, Keshet E: Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Invest 1999; 103: 159- 165.
21. Benjamin LE, Hemo I, Keshet E: A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1998; 125: 1591-1598.
22. Schrimpf C, Xin C, Campanholle G, Gill SE, Stallcup W, Lin SL, Davis GE, Gharib SA, Humphreys BD, Duffield JS: Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J Am Soc Nephrol 2012; 23: 868-883.
23. Kida Y, Ieronimakis N, Schrimpf C, Reyes M, Duffield JS: EphrinB2 reverse signaling protects against capillary rarefaction and fibrosis after kidney injury. J Am Soc Nephrol 2013; 24: 559-572.
24. Ieronimakis N, Hays AL, Janebodin K, Mahoney WM Jr, Duffield JS, Majesky MW, Reyes M: Coronary adventitial cells are linked to perivascular cardiac fibrosis via TGFβ1 signaling in the mdx mouse model of Duchenne muscular dystrophy. J Mol Cell Cardiol 2013; 63: 122-134.
25. Rajkumar VS, Howell K, Csiszar K, Denton CP, Black CM, Abraham DJ: Shared expression of phenotypic markers in systemic sclerosis indicates a convergence of pericytes and fibroblasts to a myofibroblast lineage in fibrosis. Arthritis Res Ther 2005; 7:R1113- R1123.
26. Rouget C: Memoire sur le developpement, la structure et les proprietes physiologiques des capillaries sanguins et lymphatiques. Arch Physiol Norm Pathol 1873; 5: 603-663.
27. Zimmerman K: Der feinere Bau der Blutcapillaren. Z Anat Entwicklungsgesch 1923; 68: 29-36.
28. Armulik A, Genove G, Betsholtz C: Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011; 21: 193-215.
29. Courtoy PJ, Boyles J: Fibronectin in the microvasculature: localization in the pericyteendothelial interstitium. J Ultrastruct Res 1983; 83: 258-273.
30. Sato M, Suzuki S, Senoo H: Hepatic stellate cells: unique characteristics in cell biology and phenotype. Cell Struct Funct 2003; 28: 105-112.
31. Armulik A, Genove G, Betsholtz C: Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011;21:193-215.
32. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J, Richardson C, Kopp JB, Kabir MG, Backx PH, Gerber HP, Ferrara N, Barisoni L, Alpers CE, Quaggin SE: VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 2008; 358: 1129-1136.
33. Stratman AN, Malotte KM, Mahan RD, Davis MJ, Davis GE: Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 2009; 114: 5091-5101.
34. Armulik A, Abramsson A, Betsholtz C: Endothelial/pericyte interactions. Circ Res 2005; 97: 512-523.
35. Proebstl D, Voisin MB, Woodfin A, Whiteford J, D'Acquisto F, Jones GE, Rowe D, Nourshargh S: Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. J Exp Med 2012; 209: 1219-1234.
36. Kaissling B, Hegyi I, Loffing J, Le Hir M: Morphology of interstitial cells in the healthy kidney. Anat Embryol (Berl) 1996; 193: 303- 318.
37. Rhodin JA: Ultrastructure of mammalian venous capillaries, venules, and small collecting veins. J Ultrastruct Res 1968; 25: 452-500.
38. Stark K, Eckart A, Haidari S, Tirniceriu A, Lorenz M, von Bruhl ML, Gartner F, Khandoga AG, Legate KR, Pless R, Hepper I, Lauber K, Walzog B, Massberg S: Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with pattern-recognition and motility programs. Nat Immunol 2013; 14: 41-51.
39. Davis GE, Saunders WB: Molecular balance of capillary tube formation versus regression in wound repair: role of matrix metalloproteinases and their inhibitors. J Investig Dermatol Symp Proc 2006; 11: 44-56.
40. Stratman AN, Saunders WB, Sacharidou A, Koh W, Fisher KE, Zawieja DC, Davis MJ, Davis GE: Endothelial cell lumen and vascular guidance tunnel formation requires MT1-MMP-dependent proteolysis in 3-dimensional collagen matrices. Blood 2009; 114: 237-247.
41. Saunders WB, Bohnsack BL, Faske JB, Anthis NJ, Bayless KJ, Hirschi KK, Davis GE: Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. J Cell Biol 2006; 175: 179-191.
42. Smith SW, Chand S, Savage CO: Biology of the renal pericyte. Nephrol Dial Transplant 2012; 27: 2149-2155.
43. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, Mummery C, Arthur HM, ten Dijke P: Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 2004; 23: 4018-4028.
44. Greenberg JI, Shields DJ, Barillas SG, Acevedo LM, Murphy E, Huang J, Scheppke L, Stockmann C, Johnson RS, Angle N, Cheresh DA: A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 2008; 456: 809-813.
45. Hayden MR, Karuparthi PR, Habibi J, Lastra G, Patel K, Wasekar C, Manrique CM, Ozerdem U, Stas S, Sowers JR: Ultrastructure of islet microcirculation, pericytes and the islet exocrine interface in the hip rat model of diabetes. Exp Biol Med (Maywood) 2008; 233: 1109-1123.
46. Caruso RA, Fedele F, Finocchiaro G, Pizzi G, Nunnari M, Gitto G, Fabiano V, Parisi A, Venuti A: Ultrastructural descriptions of pericyte/endothelium peg-socket interdigitations in the microvasculature of human gastric carcinomas. Anticancer Res 2009; 29: 449-453.
47. Suzuki K, Masawa N, Sakata N, Takatama M: Pathologic evidence of microvascular rarefaction in the brain of renal hypertensive rats. J Stroke Cerebrovasc Dis 2003; 12: 8-16.
48. Tilton RG, Kilo C, Williamson JR, Murch DW: Differences in pericyte contractile function in rat cardiac and skeletal muscle microvasculatures. Microvasc Res 1979; 18: 336-352.
49. Kelley C, D'Amore P, Hechtman HB, Shepro D: Microvascular pericyte contractility in vitro: comparison with other cells of the vascular wall. J Cell Biol 1987; 104: 483-490.
50. Sims DE, Miller FN, Donald A, Perricone MA: Ultrastructure of pericytes in early stages of histamine-induced inflammation. J Morphol 1990; 206: 333-342.
51. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B: A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3: 301-313.
52. Cai X, Lin Y, Friedrich CC, Neville C, Pomerantseva I, Sundback CA, Zhang Z, Vacanti JP, Hauschka PV, Grottkau BE: Bone marrow derived pluripotent cells are pericytes which contribute to vascularization. Stem Cell Rev 2009; 5: 437-445.
53. Shi S, Gronthos S: Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003; 18: 696-704.
54. Virgintino D, Girolamo F, Errede M, Capobianco C, Robertson D, Stallcup WB, Perris R, Roncali L: An intimate interplay between precocious, migrating pericytes and endothelial cells governs human fetal brain angiogenesis. Angiogenesis 2007; 10: 35-45.
55. Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C: Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 2001; 153: 543-553.
56. Amselgruber WM, Schafer M, Sinowatz F: Angiogenesis in the bovine corpus luteum: an immunocytochemical and ultrastructural study. Anat Histol Embryol 1999; 28: 157-166.
57. Ozerdem U, Stallcup WB: Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 2003; 6: 241-249.
58. Wynn TA: Cellular and molecular mechanisms of fibrosis. J Pathol 2008; 214: 199-210.
59. Shin ES, Huang Q, Gurel Z, Palenski TL, Zaitoun I, Sorenson CM, Sheibani N: STAT1- mediated Bim expression promotes the apoptosis of retinal pericytes under high glucose conditions. Cell Death Dis 2014; 5:e986.
60. Geraldes P, Hiraoka-Yamamoto J, Matsumoto M, Clermont A, Leitges M, Marette A, Aiello LP, Kern TS, King GL: Activation of PKC-delta and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy. Nat Med 2009; 15: 1298-1306.
61. Zeisberg EM, Potenta SE, Sugimoto H, Zeisberg M, Kalluri R: Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J Am Soc Nephrol 2008; 19: 2282-2287.
62. Chang L, Noseda M, Higginson M, Ly M, Patenaude A, Fuller M, Kyle AH, Minchinton AI, Puri MC, Dumont DJ, Karsan A: Differentiation of vascular smooth muscle cells from local precursors during embryonic and adult arteriogenesis requires notch signaling. Proc Natl Acad Sci USA 2012; 109: 6993- 6998.
63. Eardley KS, Kubal C, Zehnder D, Quinkler M, Lepenies J, Savage CO, Howie AJ, Kaur K, Cooper MS, Adu D, Cockwell P: The role of capillary density, macrophage infiltration and interstitial scarring in the pathogenesis of human chronic kidney disease. Kidney Int 2008; 74: 495-504.
64. Mallamaci F, Benedetto FA, Tripepi G, Cutrupi S, Pizzini P, Stancanelli B, Seminara G, Bonanno G, Rapisarda F, Fatuzzo P, Malatino LS, Zoccali C: Vascular endothelial growth factor, left ventricular dysfunction and mortality in hemodialysis patients. J Hypertens 2008; 26: 1875-1882.
65. Ohashi R, Shimizu A, Masuda Y, Kitamura H, Ishizaki M, Sugisaki Y, Yamanaka N: Peritubular capillary regression during the progression of experimental obstructive nephropathy. J Am Soc Nephrol 2002; 13: 1795-1805.
66. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C: Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999; 126: 3047-3055.
67. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A: Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380: 435- 439.
68. Betsholtz C: Insight into the physiological functions of PDGF through genetic studies in mice. Cytokine Growth Factor Rev 2004; 15: 215-228.
69. Inai T, Mancuso M, Hashizume H, Baffert F, Haskell A, Baluk P, Hu-Lowe DD, Shalinsky DR, Thurston G, Yancopoulos GD, McDonald DM: Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol 2004; 165: 35-52.
70. Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK: Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res 2004; 64: 3731-3736.
71. Lin SL, Chang FC, Schrimpf C, Chen YT, Wu CF, Wu VC, Chiang WC, Kuhnert F, Kuo CJ, Chen YM, Wu KD, Tsai TJ, Duffield JS: Targeting endothelium-pericyte crosstalk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. Am J Pathol 2011; 178: 911-923.
72. van Hinsbergh VW, Engelse MA, Quax PH: Pericellular proteases in angiogenesis and vasculogenesis. Arterioscler Thromb Vasc Biol 2006; 26: 716-728.
73. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D: Matrix metalloproteinase- 9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000; 2: 737-744.
74. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M, Kuznetsov SA, Mankani M, Robey PG, Poole AR, Pidoux I, Ward JM, Birkedal-Hansen H: MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999; 99: 81-92.
75. Cambier S, Gline S, Mu D, Collins R, Araya J, Dolganov G, Einheber S, Boudreau N, Nishimura SL: Integrin alpha(v)beta8-mediated activation of transforming growth factor- beta by perivascular astrocytes: an angiogenic control switch. Am J Pathol 2005; 166: 1883-1894.
76. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML: Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 2005; 169: 681-691.
77. Sato Y, Rifkin DB: Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J Cell Biol 1989; 109: 309-315.
78. Takata F, Dohgu S, Matsumoto J, Takahashi H, Machida T, Wakigawa T, Harada E, Miyaji H, Koga M, Nishioku T, Yamauchi A, Kataoka Y: Brain pericytes among cells constituting the blood-brain barrier are highly sensitive to tumor necrosis factor-alpha, releasing matrix metalloproteinase-9 and migrating in vitro. J Neuroinflammation 2011; 8: 106.
79. Koh W, Stratman AN, Sacharidou A, Davis GE: In vitro three dimensional collagen matrix models of endothelial lumen formation during vasculogenesis and angiogenesis. Methods Enzymol 2008; 443: 83-101.
80. Grgic I, Krautzberger AM, Hofmeister A, Lalli M, Dirocco DP, Fleig SV, Liu J, Duffield JS, McMahon AP, Aronow B, Humphreys BD: Translational profiles of medullary myofibroblasts during kidney fibrosis. J Am Soc Nephrol 2014, Epub ahead of print.
81. Wang WM, Ge G, Lim NH, Nagase H, Greenspan DS: TIMP-3 inhibits the procollagen N-proteinase ADAMTS-2. Biochem J 2006; 398: 515-519.
82. Palmer A, Zimmer M, Erdmann KS, Eulenburg V, Porthin A, Heumann R, Deutsch U, Klein R: EphrinB phosphorylation and reverse signaling: regulation by SRC kinases and PTP-BL phosphatase. Mol Cell 2002; 9: 725-737.
83. Salvucci O, Maric D, Economopoulou M, Sakakibara S, Merlin S, Follenzi A, Tosato G: EphrinB reverse signaling contributes to endothelial and mural cell assembly into vascular structures. Blood 2009; 114: 1707- 1716.
84. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH: Ephrin-B2 controls cell motility and adhesion during blood-vesselwall assembly. Cell 2006; 124: 161-173.
85. Poss KD: Advances in understanding tissue regenerative capacity and mechanisms in animals. Nat Rev Genet 2010; 11: 710-722.
86. Lin SL, Li B, Rao S, Yeo EJ, Hudson TE, Nowlin BT, Pei H, Chen L, Zheng JJ, Carroll TJ, Pollard JW, McMahon AP, Lang RA, Duffield JS: Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci USA 2010; 107: 4194-4199.
87. Bao J, Zheng JJ, Wu D: The structural basis of DKK-mediated inhibition of Wnt/LRP signaling. Sci Signal 2012; 5:pe 22.
88. Ren S, Johnson BG, Kida Y, Ip C, Davidson KC, Lin SL, Kobayashi A, Lang RA, Hadjantonakis AK, Moon RT, Duffield JS: LRP-6 is a coreceptor for multiple fibrogenic signaling pathways in pericytes and myofibroblasts that are inhibited by DKK-1. Proc Natl Acad Sci USA 2013; 110: 1440-1445.
89. DiRocco DP, Kobayashi A, Taketo MM, McMahon AP, Humphreys BD: Wnt4/betacatenin signaling in medullary kidney myofibroblasts. J Am Soc Nephrol 2013; 24: 1399- 1412.
90. Kirton JP, Crofts NJ, George SJ, Brennan K, Canfield AE: Wnt/beta-catenin signaling stimulates chondrogenic and inhibits adipogenic differentiation of pericytes: potential relevance to vascular disease? Circ Res 2007; 101: 581-589.
91. Kim MK, Maeng YI, Sung WJ, Oh HK, Park JB, Yoon GS, Cho CH, Park KK: The differential expression of TGF-beta1, ILK and wnt signaling inducing epithelial to mesenchymal transition in human renal fibrogenesis: an immunohistochemical study. Int J Clin Exp Pathol 2013; 6: 1747-1758.
92. Fang Y, Ginsberg C, Seifert M, Agapova O, Sugatani T, Register TC, Freedman BI, Monier-Faugere MC, Malluche H, Hruska KA: CKD-induced wingless/integration1 inhibitors and phosphorus cause the CKDmineral and bone disorder. J Am Soc Nephrol 2014, Epub ahead of print.
93. Ziegler T, Horstkotte J, Schwab C, Pfetsch V, Weinmann K, Dietzel S, Rohwedder I, Hinkel R, Gross L, Lee S, Hu J, Soehnlein O, Franz WM, Sperandio M, Pohl U, Thomas M, Weber C, Augustin HG, Fassler R, Deutsch U, Kupatt C: Angiopoietin 2 mediates microvascular and hemodynamic alterations in sepsis. J Clin Invest 2013, DOI: 10.1172/JCI66549.
94. Sundberg C, Kowanetz M, Brown LF, Detmar M, Dvorak HF: Stable expression of angiopoietin- 1 and other markers by cultured pericytes: phenotypic similarities to a subpopulation of cells in maturing vessels during later stages of angiogenesis in vivo. Lab Invest 2002; 82: 387-401.
95. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD: Angiopoietin-2, a natural antagonist for tie2 that disrupts in vivo angiogenesis. Science 1997; 277: 55-60.
96. Thurston G: Role of angiopoietins and tie receptor tyrosine kinases in angiogenesis and lymphangiogenesis. Cell Tissue Res 2003; 314: 61-68.
97. Augustin HG, Koh GY, Thurston G, Alitalo K: Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 2009; 10: 165- 177.
98. David S, Park JK, Meurs M, Zijlstra JG, Koenecke C, Schrimpf C, Shushakova N, Gueler F, Haller H, Kumpers P: Acute administration of recombinant angiopoietin- 1 ameliorates multiple-organ dysfunction syndrome and improves survival in murine sepsis. Cytokine 2011; 55: 251-259.
99. Hirschi KK, D'Amore PA: Pericytes in the microvasculature. Cardiovasc Res 1996; 32: 687-698.
100. Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, Diaz-Flores L Jr: Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 2009;24:909-969.
101. Takakura N, Yoshida H, Ogura Y, Kataoka H, Nishikawa S: PDGFR alpha expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal antimouse PDGFR alpha antibody APA5. J Histochem Cytochem 1997;45:883-893.
102. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, Alvarez-Buylla A: PDGFR alphapositive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006;51:187-199.
103. Bergers G, Song S: The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 2005;7:452-464.
104. Ruiter DJ, Schlingemann RO, Westphal JR, Denijn M, Rietveld FJ, De Waal RM: Angiogenesis in wound healing and tumor metastasis. Behring Inst Mitt 1993:258-272.
105. Huang FJ, You WK, Bonaldo P, Seyfried TN, Pasquale EB, Stallcup WB: Pericyte deficiencies lead to aberrant tumor vascularizaton in the brain of the NG2 null mouse. Dev Biol 2010; 344:1035-1046.
106. Nehls V, Denzer K, Drenckhahn D: Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res 1992; 270:469-474.
107. Strutz F, Zeisberg M: Renal fibroblasts and myofibroblasts in chronic kidney disease. J Am Soc Nephrol 2006;17:2992-2998.
108. Bondjers C, Kalen M, Hellstrom M, Scheidl SJ, Abramsson A, Renner O, Lindahl P, Cho H, Kehrl J, Betsholtz C: Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells. Am J Pathol 2003; 162:721-729.
109. MacFadyen JR, Haworth O, Roberston D, Hardie D, Webster MT, Morris HR, Panico M, Sutton-Smith M, Dell A, van der Geer P, Wienke D, Buckley CD, Isacke CM: Endosialin (TEM1, CD248) is a marker of stromal fibroblasts and is not selectively expressed on tumour endothelium. FEBS Lett 2005; 579:2569-2575.
110. Smith SW, Eardley KS, Croft AP, Nwosu J, Howie AJ, Cockwell P, Isacke CM, Buckley CD, Savage CO: CD248+ stromal cells are associated with progressive chronic kidney disease. Kidney Int 2011;80:199-207.
111. Dermietzel R, Krause D: Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry. Int Rev Cytol 1991; 127:57-109.
112. Kunz J, Krause D, Kremer M, Dermietzel R: The 140-kDa protein of blood-brain barrierassociated pericytes is identical to aminopeptidase N. J Neurochem 1994;62:2375- 2386.
113. Stefanovic V, Vlahovic P, Ardaillou N, Ronco P, Ardaillou R: Cell surface aminopeptidase A and N activities in human glomerular epithelial cells. Kidney Int 1992; 41:1571- 1580.
114. Nassiri F, Cusimano MD, Scheithauer BW, Rotondo F, Fazio A, Yousef GM, Syro LV, Kovacs K, Lloyd RV: Endoglin (CD105): a review of its role in angiogenesis and tumor diagnosis, progression and therapy. Anticancer Res 2011;31:2283-2290.
115. Pierelli L, Bonanno G, Rutella S, Marone M, Scambia G, Leone G: CD105 (endoglin) expression on hematopoietic stem/progenitor cells. Leuk Lymphoma 2001;42:1195-1206.
116. Sackstein R, Merzaban JS, Cain DW, Dagia NM, Spencer JA, Lin CP, Wohlgemuth R: Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 2008; 14:181-187.
117. Jalkanen S, Jalkanen M: Lymphocyte CD44 binds the COOH-terminal heparin-binding domain of fibronectin. J Cell Biol 1992; 116:817-825.
118. Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R: CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 2001;153:1277-1286.
119. Sato A, Iwama A, Takakura N, Nishio H, Yancopoulos GD, Suda T: Characterization of TEK receptor tyrosine kinase and its ligands, Angiopoietins, in human hematopoietic progenitor cells. Int Immunol 1998; 10:1217-1227.
120. Stratmann A, Risau W, Plate KH: Cell typespecific expression of angiopoietin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. Am J Pathol 1998;153: 1459-1466.
121. Nakayama T, Yao L, Tosato G: Mast cell-derived angiopoietin-1 plays a critical role in the growth of plasma cell tumors. J Clin Invest 2004;114:1317-1325.
122. Berse B, Brown LF, Van de Water L, Dvorak HF, Senger DR: Vascular permeability factor (vascular endothelial growth factor) gene is expressed differentially in normal tissues, macrophages, and tumors. Mol Biol Cell 1992;3:211-220.