Resident mesenchymal cells and fibrosis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 7, 2013, Pages 962-971

  Hutchison, Nicol ^a,b   Fligny, Cécile ^a,b   Duffield, Jeremy S ^a,b  

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

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anti fibrotic therapeutics; Fibrillar extracellular matrix; Fibrosis; Myofibroblast; Pericyte; Resident mesenchymal cell

Indexed keywords

CD31 ANTIGEN; COLLAGEN TYPE 1; LAMININ ALPHA4;

ADAPTIVE IMMUNITY; BLOOD CLOTTING; BONE MARROW CELL; CAPILLARY; CAPILLARY BASEMENT MEMBRANE; CAUSE OF DEATH; CELL ACTIVATION; CELL FUNCTION; CELL INTERACTION; CELL POPULATION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; DERMIS; DIABETES MELLITUS; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROGENESIS; FIBROSIS; HUMAN; IMMUNOCOMPETENT CELL; INFECTION; INNATE IMMUNITY; INTERSTITIUM; KIDNEY; MESENCHYME CELL; MICROVASCULATURE; MYOFIBROBLAST; NEUTROPHIL CHEMOTAXIS; NONHUMAN; ORGAN INJURY; PERICYTE; PRIORITY JOURNAL; RESIDENT MESENCHYMAL CELL; REVIEW; SCAR FORMATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TISSUE REGENERATION; VASCULAR DISEASE; WOUND HEALING; MESENCHYMAL STROMA CELL;

FIBROBLASTS; FIBROSIS; HUMANS; MESENCHYMAL STROMAL CELLS; MYOFIBROBLASTS; PERICYTES;

EID: 84877064532     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.11.015     Document Type: Review

References (90)

1. Wynn T.A. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J. Clin. Invest. 2007, 117:524-529.
2. Bellomo R., Kellum J.A., Ronco C. Acute kidney injury. Lancet 2012, 380:756-766.
3. Selman M., Rojas M., Mora A., Pardo A. Aging and interstitial lung diseases: unraveling an old forgotten player in the pathogenesis of lung fibrosis. Semin. Respir. Crit. Care Med. 2010, 31:607-617.
4. Monroe D.M., Hoffman M. The clotting system - a major player in wound healing. Haemophilia 2012, 18:11-16.
5. Salloum S., Tai A.W. Treating hepatitis C infection by targeting the host. Transl. Res. 2012, 159:421-429.
6. Gabbiani G., Majno G. Dupuytren's contracture: fibroblast contraction? An ultrastructural study. Am. J. Pathol. 1972, 66:131-146.
7. Ross R., Everett N.B., Tyler R. Wound healing and collagen formation. VI. The origin of the wound fibroblast studied in parabiosis. J. Cell Biol. 1970, 44:645-654.
8. Skalli O., Schürch W., Seemayer T., Lagacé R., Montandon D., Pittet B., Gabbiani G. Myofibroblasts from diverse pathologic settings are heterogeneous in their content of actin isoforms and intermediate filament proteins. Lab. Invest. 1989, 60:275-285.
9. Darby I., Skalli O., Gabbiani G. Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab. Invest. 1990, 63:21-29.
10. Hinz B., Celetta G., Tomasek J.J., Gabbiani G., Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol. Biol. Cell 2001, 12:2730-2741.
11. Hinz B., Mastrangelo D., Iselin C.E., Chaponnier C., Gabbiani G. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am. J. Pathol. 2001, 159:1009-1020.
12. Katoh K., Kano Y., Amano M., Onishi H., Kaibuchi K., Fujiwara K. Rho-kinase-mediated contraction of isolated stress fibers. J. Cell Biol. 2001, 153:569-584.
13. Bogatkevich G.S., Tourkina E., Abrams C.S., Harley R.A., Silver R.M., Ludwicka-Bradley A. Contractile activity and smooth muscle alpha-actin organization in thrombin-induced human lung myofibroblasts. Am. J. Physiol. Lung Cell Mol. Physiol. 2003, 285:L334-43.
14. Picard N., Baum O., Vogetseder A., Kaissling B., Le Hir M. Origin of renal myofibroblasts in the model of unilateral ureter obstruction in the rat. Histochem. Cell Biol. 2008, 130:141-155.
15. Desmoulière A., Chaponnier C., Gabbiani G. Tissue repair, contraction, and the myofibroblast. Wound Repair Regen. 2005, 13:7-12.
16. Strutz F., Zeisberg M., Hemmerlein B., Sattler B., Hummel K., Becker V., Müller G.A. Basic fibroblast growth factor expression is increased in human renal fibrogenesis and may mediate autocrine fibroblast proliferation. Kidney Int. 2000, 57:1521-1538.
17. Sharpe C.C., Dockrell M.E., Noor M.I., Monia B.P., Hendry B.M. Role of Ras isoforms in the stimulated proliferation of human renal fibroblasts in primary culture. J. Am. Soc. Nephrol. 2000, 11:1600-1606.
18. Kisseleva T., Cong M., Paik Y., Scholten D., Jiang C., Benner C., Iwaisako K., Moore-Morris T., Scott B., Tsukamoto H., Evans S.M., Dillmann W., Glass C.K., Brenner D.A. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc. Natl. Acad. Sci. 2012, 109:9448-9453.
19. Humphreys B.D., Lin S.-L., Kobayashi A., Hudson T.E., Nowlin B.T., Bonventre J.V., Valerius M.T., McMahon A.P., Duffield J.S. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 2010, 176:85-97.
20. Göritz C., Dias D.O., Tomilin N., Barbacid M., Shupliakov O., Frisén J. A pericyte origin of spinal cord scar tissue. Science 2011, 333:238-242.
21. Lin S.-L., Kisseleva T., Brenner D.A., Duffield J.S. 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.
22. Rock J.R., Barkauskas C.E., Cronce M.J., Xue Y., Harris J.R., Liang J., Noble P.W., Hogan B.L.M. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc. Natl. Acad. Sci. 2011, 108:E1475-83.
23. Murphy M.M., Lawson J.A., Mathew S.J., Hutcheson D.A., Kardon G. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 2011, 138:3625-3637.
24. Mathew S.J., Hansen J.M., Merrell A.J., Murphy M.M., Lawson J.A., Hutcheson D.A., Hansen M.S., Angus-Hill M., Kardon G. Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development 2011, 138:371-384.
25. Sponheim J., Pollheimer J., Olsen T., Balogh J., Hammarström C., Loos T., Kasprzycka M., Sørensen D.R., Nilsen H.R., Küchler A.M., Vatn M.H., Haraldsen G. Inflammatory bowel disease-associated interleukin-33 is preferentially expressed in ulceration-associated myofibroblasts. Am. J. Pathol. 2010, 177:2804-2815.
26. Acharya A., Baek S.T., Huang G., Eskiocak B., Goetsch S., Sung C.Y., Banfi S., Sauer M.F., Olsen G.S., Duffield J.S., Olson E.N., Tallquist M.D. The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors. Development 2012, 139:2139-2149.
27. Sato M., Suzuki S., Senoo H. Hepatic stellate cells: unique characteristics in cell biology and phenotype. Cell Struct. Funct. 2003, 28:105-112.
28. Lee J.S., Semela D., Iredale J., Shah V.H. Sinusoidal remodeling and angiogenesis: a new function for the liver-specific pericyte?. Hepatology 2007, 45:817-825.
29. Kaissling B., Le Hir M. The renal cortical interstitium: morphological and functional aspects. Histochem. Cell Biol. 2008, 130:247-262.
30. Lin S.L., Chang F.C., Schrimpf C., Chen Y.T., Wu C.F., Wu V.C., Chiang W.C., Kuhnert F., Kuo C.J., Chen Y.M., Wu K.D., Tsai T.J., Duffield J.S. Targeting endothelium-pericyte cross talk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction and fibrosis. Am. J. Pathol. 2011, 178:911-923.
31. Qiao J., Sakurai H., Nigam S.K. Branching morphogenesis independent of mesenchymal-epithelial contact in the developing kidney. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:7330-7335.
32. Stark K., Vainio S., Vassileva G., McMahon A.P. Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 1994, 372:679-683.
33. Horster M., Huber S., Tschöp J., Dittrich G., Braun G. Epithelial nephrogenesis. Pflugers Arch. 1997, 434:647-660.
34. Taura K., Miura K., Iwaisako K., Osterreicher C.H., Kodama Y., Penz-Osterreicher M., Brenner D.A. Hepatocytes do not undergo epithelial-mesenchymal transition in liver fibrosis in mice. Hepatology 2010, 51:1027-1036.
35. Koesters R., Kaissling B., Lehir M., Picard N., Theilig F., Gebhardt R., Glick A.B., Hähnel B., Hosser H., Gröne H.-J., Kriz W. Tubular overexpression of transforming growth factor-beta1 induces autophagy and fibrosis but not mesenchymal transition of renal epithelial cells. Am. J. Pathol. 2010, 177:632-643.
36. Chu A.S., Diaz R., Hui J.-J., Yanger K., Zong Y., Alpini G., Stanger B.Z., Wells R.G. Lineage tracing demonstrates no evidence of cholangiocyte epithelial-to-mesenchymal transition in murine models of hepatic fibrosis. Hepatology 2011, 53:1685-1695.
37. Armulik A., Genové G., Mäe M., Nisancioglu M.H., Wallgard E., Niaudet C., He L., Norlin J., Lindblom P., Strittmatter K., Johansson B.R., Betsholtz C. Pericytes regulate the blood-brain barrier. Nature 2010, 468:557-561.
38. Winau F., Hegasy G., Weiskirchen R., Weber S., Cassan C., Sieling P.A., Modlin R.L., Liblau R.S., Gressner A.M., Kaufmann S.H.E. Ito cells are liver-resident antigen-presenting cells for activating T cell responses. Immunity 2007, 26:117-129.
39. Grillo H.C. Origin of fibroblasts in wound healing An autoradiographic study of inhibition of cellular proliferation by local X-irradiation. Ann. Surg. 1963, 157:453-467.
40. Dulauroy S., Di Carlo S.E., Langa F., Eberl G.E.R., 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.
41. Asada N., Takase M., Nakamura J., Oguchi A., Asada M., Suzuki N., Yamamura K.-I., Nagoshi N., Shibata S., Rao T.N., Fehling H.J., Fukatsu A., Minegishi N., Kita T., Kimura T., Okano H., Yamamoto M., Yanagita M. Dysfunction of fibroblasts of extrarenal origin underlies renal fibrosis and renal anemia in mice. J. Clin. Invest. 2011, 121:3981-3990.
42. Cohnheim J.F. Ueber entzundung und eiterung. Path. Anat. Physiol. Klin. Med. 1867, 40:1-79.
43. Joe A.W.B., Yi L., Natarajan A., Le Grand F., So L., Wang J., Rudnicki M.A., Rossi F.M.V. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 2010, 12:153-163.
44. Uezumi A., Fukada S.-I., Yamamoto N., Takeda S., Tsuchida K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 2010, 12:143-152.
45. Uezumi A., Ito T., Morikawa D., Shimizu N., Yoneda T., Segawa M., Yamaguchi M., Ogawa R., Matev M.M., Miyagoe-Suzuki Y., Takeda S., Tsujikawa K., Tsuchida K., Yamamoto H., Fukada S.I. Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. J. Cell Sci. 2011, 124:3654-3664.
46. Olson L.E., Soriano P. Increased PDGFRα activation disrupts connective tissue development and drives systemic fibrosis. Dev. Cell 2009, 16:303-313.
47. Olson L.E., Soriano P. PDGFRβ signaling regulates mural cell plasticity and inhibits fat development. Dev. Cell 2011, 20:815-826.
48. Friedman S.L., Roll F.J., Boyles J., Bissell D.M. Hepatic lipocytes: the principal collagen-producing cells of normal rat liver. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:8681-8685.
49. Friedman S.L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 2008, 88:125-172.
50. Kisseleva T., Brenner D.A. The phenotypic fate and functional role for bone marrow-derived stem cells in liver fibrosis. J. Hepatol. 2012, 56:965-972.
51. Friedman S.L. Evolving challenges in hepatic fibrosis. Nat. Rev. Gastroenterol. Hepatol. 2010, 7:425-436.
52. Reynaert H., Thompson M.G., Thomas T., Geerts A. Hepatic stellate cells: role in microcirculation and pathophysiology of portal hypertension. Gut 2002, 50:571-581.
53. Housset C., Rockey D.C., Bissell D.M. Endothelin receptors in rat liver: lipocytes as a contractile target for endothelin 1. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:9266-9270.
54. Görbig M.N., Ginès P., Bataller R., Nicolás J.M., Garcia-Ramallo E., Tobías E., Titos E., Rey M.J., Clària J., Arroyo V., Rodés J. Atrial natriuretic peptide antagonizes endothelin-induced calcium increase and cell contraction in cultured human hepatic stellate cells. Hepatology 1999, 30:501-509.
55. Loureiro-Silva M.R., Cadelina G.W., Groszmann R.J. Deficit in nitric oxide production in cirrhotic rat livers is located in the sinusoidal and postsinusoidal areas. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 284:G567-74.
56. Bataller R., Sancho-Bru P., Ginès P., Brenner D.A. Liver fibrogenesis: a new role for the renin-angiotensin system. Antioxid. Redox Signal. 2005, 7:1346-1355.
57. Rouget C. Mémoire sur le dévelopement, la structure et les propriétés physiologiques des capillaires sanguins et lymphatiques. Arch. Physiol. Norm. Pathol. 1873, 5:603-633.
58. Daneman R., Zhou L., Kebede A.A., Barres B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010, 468:562-566.
59. Krueger M., Bechmann I. CNS pericytes: concepts, misconceptions, and a way out. Glia 2010, 58:1-10.
60. Armulik A. Endothelial/pericyte interactions. Circ. Res. 2005, 97:512-523.
61. von Tell D., Armulik A., Betsholtz C. Pericytes and vascular stability. Exp. Cell Res. 2006, 312:623-629.
62. Mogensen C., Bergner B., Wallner S., Ritter A., d'Avis S., Ninichuk V., Kameritsch P., Gloe T., Nagel W., Pohl U. Isolation and functional characterization of pericytes derived from hamster skeletal muscle. Acta Physiol. (Oxf.) 2011, 201:413-426.
63. Sundberg C., Kowanetz M., Brown L.F., Detmar M., Dvorak H.F. 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.
64. Gerlach J.C., Over P., Turner M.E., Thompson R.L., Foka H.G., Chen W.C.W., Péault B., Gridelli B., Schmelzer E. Perivascular mesenchymal progenitors in human fetal and adult liver. Stem Cells Dev. 2012, (121016061216008).
65. Schrimpf C., Xin C., Campanholle G., Gill S.E., Stallcup W., Lin S.-L., Davis G.E., Gharib S.A., Humphreys B.D., Duffield J.S. Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J. Am. Soc. Nephrol. 2012, 23:868-883.
66. Stratman A.N., Schwindt A.E., Malotte K.M., Davis G.E. Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilization. Blood 2010, 116:4720-4730.
67. Kutcher M.E., Kolyada A.Y., Surks H.K., Herman I.M. Pericyte Rho GTPase mediates both pericyte contractile phenotype and capillary endothelial growth state. Am. J. Pathol. 2007, 171:693-701.
68. Ridley A.J. Historical overview of Rho GTPases. Methods Mol. Biol. 2012, 827:3-12.
69. Stratman A.N., Malotte K.M., Mahan R.D., Davis M.J., Davis G.E. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 2009, 114:5091-5101.
70. Fukuda K., Yoshitomi K., Yanagida T., Tokumoto M., Hirakata H. Quantification of TGF-beta1 mRNA along rat nephron in obstructive nephropathy. Am. J. Physiol. Renal. Physiol. 2001, 281:F513-21.
71. Floege J., Eitner F., Alpers C.E. A new look at platelet-derived growth factor in renal disease. J. Am. Soc. Nephrol. 2008, 19:12-23.
72. Ma L.-J., Yang H., Gaspert A., Carlesso G., Barty M.M., Davidson J.M., Sheppard D., Fogo A.B. Transforming growth factor-beta-dependent and -independent pathways of induction of tubulointerstitial fibrosis in beta6(-/-) mice. Am. J. Pathol. 2003, 163:1261-1273.
73. Moyano J.V., Greciano P.G., Buschmann M.M., Koch M., Matlin K.S. Autocrine transforming growth factor-{beta}1 activation mediated by integrin {alpha}V{beta}3 regulates transcriptional expression of laminin-332 in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 2010, 21:3654-3668.
74. Hahm K., Lukashev M.E., Luo Y., Yang W.J., Dolinski B.M., Weinreb P.H., Simon K.J., Chun Wang L., Leone D.R., Lobb R.R., McCrann D.J., Allaire N.E., Horan G.S., Fogo A., Kalluri R., Shield C.F., Sheppard D., Gardner H.A., Violette S.M. Alphav beta6 integrin regulates renal fibrosis and inflammation in Alport mouse. Am. J. Pathol. 2007, 170:110-125.
75. Sato M., Muragaki Y., Saika S., Roberts A.B., Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J. Clin. Invest. 2003, 112:1486-1494.
76. Wang S., Wilkes M.C., Leof E.B., Hirschberg R. Noncanonical TGF-beta pathways, mTORC1 and Abl, in renal interstitial fibrogenesis. Am. J. Physiol. Renal. Physiol. 2010, 298:F142-9.
77. El Chaar M., Chen J., Seshan S.V., Jha S., Richardson I., Ledbetter S.R., Vaughan E.D., Poppas D.P., Felsen D. Effect of combination therapy with enalapril and the TGF-beta antagonist 1D11 in unilateral ureteral obstruction. Am. J. Physiol. Renal. Physiol. 2007, 292:F1291-301.
78. Wang S., Wilkes M.C., Leof E.B., Hirschberg R. Imatinib mesylate blocks a non-Smad TGF-beta pathway and reduces renal fibrogenesis in vivo. FASEB J. 2005, 19:1-11.
79. Traykova-Brauch M., Schönig K., Greiner O., Miloud T., Jauch A., Bode M., Felsher D.W., Glick A.B., Kwiatkowski D.J., Bujard H., Horst J., von Knebel Doeberitz M., Niggli F.K., Kriz W., Gröne H.-J., Koesters R. An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nat. Med. 2008, 14:979-984.
80. Wu C.-F., Chiang W.-C., Lai C.-F., Chang F.-C., Chen Y.-T., Chou Y.-H., Wu T.-H., Linn G.R., Ling H., Wu K.-D., Tsai T.-J., Chen Y.-M., Duffield J.S., Lin S.-L. Transforming growth factor β-1 stimulates profibrotic epithelial signaling to activate pericyte-myofibroblast transition in obstructive kidney fibrosis. Am. J. Pathol. 2012, 1-15.
81. Seki E., De Minicis S., Gwak G.-Y., Kluwe J., Inokuchi S., Bursill C.A., Llovet J.M., Brenner D.A., Schwabe R.F. CCR1 and CCR5 promote hepatic fibrosis in mice. J. Clin. Invest. 2009, 119:1858-1870.
82. Schuppan D., Pinzani M. Anti-fibrotic therapy: lost in translation?. J. Hepatol. 2012, 56:S66-S74.
83. Dussaule J.-C., Guerrot D., Huby A.-C., Chadjichristos C., Shweke N., Boffa J.-J., Chatziantoniou C. The role of cell plasticity in progression and reversal of renal fibrosis. Int. J. Exp. Pathol. 2011, 92:151-157.
84. Ronco P., Chatziantoniou C. Matrix metalloproteinases and matrix receptors in progression and reversal of kidney disease: therapeutic perspectives. Kidney Int. 2008, 74:873-878.
85. Bouros D. Pirfenidone for idiopathic pulmonary fibrosis. Lancet 2011, 377:1727-1729.
86. Nakanishi H., Sugiura T., Streisand J.B., Lonning S.M., Roberts J.D. TGF-beta-neutralizing antibodies improve pulmonary alveologenesis and vasculogenesis in the injured newborn lung. Am. J. Physiol. Lung Cell Mol. Physiol. 2007, 293:L151-61.
87. Trachtman H., Fervenza F.C., Gipson D.S., Heering P., Jayne D.R.W., Peters H., Rota S., Remuzzi G., Rump L.C., Sellin L.K., Heaton J.P.W., Streisand J.B., Hard M.L., Ledbetter S.R., Vincenti F. A phase 1, single-dose study of fresolimumab, an anti-TGF-β antibody, in treatment-resistant primary focal segmental glomerulosclerosis. Kidney Int. 2011, 79:1236-1243.
88. Kay J., High W.A. Imatinib mesylate treatment of nephrogenic systemic fibrosis. Arthritis Rheum. 2008, 58:2543-2548.
89. Adler S.G., Schwartz S., Williams M.E., Arauz-Pacheco C., Bolton W.K., Lee T., Li D., Neff T.B., Urquilla P.R., Sewell K.L. Phase 1 study of anti-CTGF monoclonal antibody in patients with diabetes and microalbuminuria. Clin. J. Am. Soc. Nephrol. 2010, 5:1420-1428.
90. Duffield J.S., Lupher M., Thannickal V.J., Wynn T.A. Host responses in tissue repair and fibrosis. Annu. Rev. Pathol. Mech. Dis. 2012, 8. (121023133009008).