Role of lung Pericytes and resident fibroblasts in the pathogenesis of pulmonary fibrosis

American Journal of Respiratory and Critical Care Medicine

Volumn 188, Issue 7, 2013, Pages 820-830

  Hung, Chi ^a,c   Linn, Geoffrey ^a,b,c   Chow, Yu Hua ^a,c   Kobayashi, Akio ^b,d   Mittelsteadt, Kristen ^a,c   Altemeier, William A ^a,c   Gharib, Sina A ^a,c   Schnapp, Lynn M ^a,c   Duffield, Jeremy S ^a,b,c  

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

^b Renal Division   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Fibrosis; Foxd1; Lung injury; Myofibroblast; Pericyte

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; FIBRILLAR COLLAGEN; MEMBRANE PROTEIN; PROTEIN FOXD1; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE LOCUS; INNATE IMMUNITY; LUNG FIBROBLAST; LUNG FIBROSIS; LUNG INJURY; MESENCHYME CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PATHOGENESIS; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; BLEOMYCIN; FORKHEAD TRANSCRIPTION FACTORS; LUNG INJURY; MESENCHYMAL STROMAL CELLS; MICE; MYOFIBROBLASTS; PERICYTES; PULMONARY FIBROSIS;

EID: 84886304100     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201212-2297OC     Document Type: Article

References (44)

1. Brewster CE, Howarth PH, Djukanovic R, Wilson J, Holgate ST, Roche WR. Myofibroblasts and subepithelial fibrosis in bronchial asthma. Am J Respir Cell Mol Biol 1990;3:507-511.
2. Roche WR, Beasley R, Williams JH, Holgate ST. Subepithelial fibrosis in the bronchi of asthmatics. Lancet 1989;1:520-524. (Pubitemid 19075206)
3. Raghu G, Weycker D, Edelsberg J, Bradford WZ, Oster G. Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2006;174:810-816. (Pubitemid 44511663)
4. Luppi F, Spagnolo P, Cerri S, Richeldi L. The big clinical trials in idiopathic pulmonary fibrosis. Curr Opin Pulm Med 2012;18:428-432.
5. Fernandez IE, Eickelberg O. New cellular and molecular mechanisms of lung injury and fibrosis in idiopathic pulmonary fibrosis. Lancet 2012; 380:680-688.
6. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, Harris JR, Liang J, Noble PW, Hogan BL. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci US.A. 2011;108:E1475-E1483.
7. Scholten D, Osterreicher CH, Scholten A, Iwaisako K, Gu G, Brenner DA, Kisseleva T. Genetic labeling does not detect epithelial-tomesenchymal transition of cholangiocytes in liver fibrosis in mice. Gastroenterology 2010;139:987-998.
8. Levine D, Rockey DC, Milner TA, Breuss JM, Fallon JT, Schnapp LM. Expression of the integrin alpha8beta1 during pulmonary and hepatic fibrosis. Am J Pathol 2000;156:1927-1935. (Pubitemid 30641762)
9. 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.
10. Koesters R, Kaissling B, Lehir M, Picard N, Theilig F, Gebhardt R, Glick AB, Hähnel B, Hosser H, Gröne HJ, et al. 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.
11. Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro-oncol 2005;7:452-464. (Pubitemid 41555617)
12. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011;21: 193-215.
13. Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 2011;138:3625-3637.
14. Schrimpf C, Duffield JS. Mechanisms of fibrosis: the role of the pericyte. Curr Opin Nephrol Hypertens 2011;20:297-305.
15. 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 2010;176:85-97.
16. Göritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisén J. A pericyte origin of spinal cord scar tissue. Science 2011;333:238-242.
17. Apte MV, Haber PS, Applegate TL, Norton ID, McCaughan GW, Korsten M.A., Pirola RC, Wilson JS. Periacinar stellate shaped cells in rat pancreas: identification, isolation, and culture. Gut 1998;43:128-133. (Pubitemid 28335501)
18. Mathew SJ, Hansen JM, Merrell AJ, Murphy MM, Lawson JA, Hutcheson DA, Hansen MS, Angus-Hill M, Kardon G. Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development 2011; 138:371-384.
19. Sponheim J, Pollheimer J, Olsen T, Balogh J, Hammarström C, Loos T, Kasprzycka M, Sørensen DR, Nilsen HR, Küchler AM, et al. Inflammatory bowel disease-associated interleukin-33 is preferentially expressed in ulceration-associated myofibroblasts. Am J Pathol 2010;177:2804-2815.
20. Schrimpf C, Xin C, Campanholle G, Gill SE, Stallcup W, Lin SL, Davis GE, Gharib S.A., Humphreys BD, Duffield JS. Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J Am Soc Nephrol 2012;23:868-883.
21. Zhang H, Palmer R, Gao X, Kreidberg J, Gerald W, Hsiao L, Jensen RV, Gullans SR, Haber DA. Transcriptional activation of placental growth factor by the forkhead/winged helix transcription factor FoxD1. Curr Biol 2003;13:1625-1629. (Pubitemid 37215887)
22. Hung CF, Linn GR, Chow Y, Kobayashi A, Duffield JS, Schnapp LM. Pericyte-like cells and resident fibroblasts are sources of myofibroblasts in acute lung injury. Am J Respir Crit Care Med 2012;185: A6805.
23. Hung CF, Chow Y, Gharib S.A., Duffield JS, Schnapp LM. Lung stromal cell diversity identified by transcriptional profiling. Am J Respir Crit Care Med 2013;187:A3827.
24. Krempen K, Grotkopp D, Hall K, Bache A, Gillan A, Rippe R.A., Brenner DA, Breindl M. Far upstream regulatory elements enhance position-independent and uterus-specific expression of the murine alpha1(I) collagen promoter in transgenic mice. Gene Expr 1999;8: 151-163.
25. Yata Y, Scanga A, Gillan A, Yang L, Reif S, Breindl M, Brenner DA, Rippe R.A.. DNase I-hypersensitive sites enhance alpha1(I) collagen gene expression in hepatic stellate cells. Hepatology 2003;37:267-276. (Pubitemid 36152525)
26. Lin S-L, Chang F-C, Schrimpf C, Chen Y-T, Wu C-F, Wu V-C, Chiang W-C, Kuhnert F, Cuo CJ, Chen Y-M, et al. Targeting endotheliumpericyte crosstalk by inhibiting VEGF receptor signaling attenuates kidney microvascular rarefaction & fibrosis. Am J Pathol 2011;178: 911-923.
27. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res 2005;97:512-523. (Pubitemid 41361741)
28. Krueger M, Bechmann I. CNS pericytes: concepts, misconceptions, and a way out. Glia 2010;58:1-10.
29. Nehls V, Drenckhahn D. Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin. J Cell Biol 1991;113:147-154. (Pubitemid 21909681)
30. Miller M.F., Cohen ED, Baggs JE, Lu MM, Hogenesch JB, Morrisey EE. Wnt ligands signal in a cooperative manner to promote foregut organogenesis. Proc Natl Acad Sci US.A. 2012;109:15348-15353.
31. Peng T, Tian Y, Boogerd CJ, Lu MM, Kadzik RS, Stewart KM, Evans SM, Morrisey EE. Coordination of heart and lung co-development by a multipotent cardiopulmonary progenitor. Nature 2013;500: 589-592.
32. Chen YT, Chang FC, Wu CF, Chou YH, Hsu HL, Chiang WC, Shen J, Chen YM, Wu KD, Tsai TJ, et al. Platelet-derived growth factor receptor signaling activates pericyte-myofibroblast transition in obstructive and post-ischemic kidney fibrosis. Kidney Int 2011;80:1170-1181.
33. Wu CF, Chiang WC, Lai CF, Chang FC, Chen YT, Chou YH, Wu TH, Linn GR, Ling H, Wu KD, et al. Transforming growth factor b-1 stimulates profibrotic epithelial signaling to activate pericytemyofibroblast transition in obstructive kidney fibrosis. Am J Pathol 2013;182:118-131.
34. Duffield JS. The elusive source of myofibroblasts: problem solved? Nat Med 2012;18:1178-1180.
35. Campanholle G, Ligresti G, Gharib S.A., Duffield JS. Cellular mechanisms of tissue fibrosis. 3. Novel mechanisms of kidney fibrosis. Am J Physiol Cell Physiol 2013;304:C591-C603.
36. Kida Y, Duffield JS. Pivotal role of pericytes in kidney fibrosis. Clin Exp Pharmacol Physiol 2011;38:467-473.
37. Olson LE, Soriano P. PDGFRb signaling regulates mural cell plasticity and inhibits fat development. Dev Cell 2011;20:815-826.
38. Voisin MB, Nourshargh S. Neutrophil transmigration: emergence of an adhesive cascade within venular walls. J Innate Immun 2013;5:336-347.
39. Alon R, Nourshargh S. Learning in motion: pericytes instruct migrating innate leukocytes. Nat Immunol 2013;14:14-15.
40. 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 ExpMed 2012;209: 1219-1234.
41. Campanholle G, Chen CL,Mittelsteadt K, Kobayashi A, Lin S-L, Gharib S.A., Heinecke J, Hamerman JA, AltemeierWA, Duffield JS. Trem-1, tlr-2 and tlr-4 are dispensable in kidney macrophages. PLoS ONE (In press)
42. Gerlach JC, Over P, Turner ME, Thompson RL, Foka HG, Chen WC, Péault B, Gridelli B, Schmelzer E. Perivascular mesenchymal progenitors in human fetal and adult liver. Stem Cells Dev 2012;21: 3258-3269.
43. Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, Delbono O. Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev 2013;22:2298-2314.
44. Blocki A, Wang Y, Koch M, Peh P, Beyer S, Law P, Hui J, Raghunath M. Not all MSCS can act as pericytes: Functional in vitro assays to distinguish pericytes from other mesenchymal stem cells in angiogenesis. Stem Cells Dev 2013;22:2347-2355.