Thy-1 signals through PPARγ to promote lipofibroblast differentiation in the developing lung

American Journal of Respiratory Cell and Molecular Biology

Volumn 46, Issue 6, 2012, Pages 765-772

  Varisco, Brian M ^a   Ambalavanan, Namasivayam ^b   Whitsett, Jeffrey A ^a   Hagood, James S ^c  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b University of Alabama at Birmingham   (United States)

^c RADY CHILDREN'S HOSPITAL   (United States)

Author keywords

Lipid metabolism; Lipofibroblast; PPAR ; Thy 1

Indexed keywords

BETA ACTIN; CELL SURFACE PROTEIN; CIGLITAZONE; FATTY ACID; FATTY ACID TRANSPORTER; FATTY ACID TRANSPORTER PROTEIN 3; GLYCOSYLPHOSPHATIDYLINOSITOL; LIPID; LIVER X RECEPTOR ALPHA; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROSTAGLANDIN J2; RETINOID RELATED ORPHAN RECEPTOR ALPHA; THY 1 ANTIGEN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADIPOCYTE; ALVEOLARIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ESTERIFICATION; FATTY ACID TRANSPORT; HOMEOSTASIS; IN VIVO STUDY; LUNG ALVEOLUS; LUNG DEVELOPMENT; LUNG FIBROBLAST; LUNG LIPOFIBROBLAST; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, THY-1; CELL DIFFERENTIATION; ESTERIFICATION; FIBROBLASTS; LUNG; MICE; MICE, INBRED C57BL; PPAR GAMMA; SIGNAL TRANSDUCTION;

EID: 84861791200     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2011-0316OC     Document Type: Article

References (48)

1. Zoetis T, Hurtt ME. Species comparison of lung development. Birth Defects Res B Dev Reprod Toxicol 2003;68:121-124. (Pubitemid 38222009)
2. Balinotti JE, Tiller CJ, Llapur CJ, Jones MH, Kimmel RN, Coates CE, Katz BP, Nguyen JT, Tepper RS. Growth of the lung parenchyma early in life. Am J Respir Crit Care Med 2009;179:134-137.
3. Hislop AA, Wigglesworth JS, Desai R. Alveolar development in the human fetus and infant. Early Hum Dev 1986;13:1-11. (Pubitemid 16124138)
4. Baraldi E, Filippone M. Chronic lung disease after premature birth. N Engl J Med 2007;357:1946-1955. (Pubitemid 350074689)
5. Kobaly K, Schluchter M, Minich N, Friedman H, Taylor HG, Wilson-Costello D, Hack M. Outcomes of extremely low birth weight (<1 kg) and extremely low gestational age (<28 weeks) infants with bronchopulmonary dysplasia: effects of practice changes in 2000 to 2003. Pediatrics 2008;121:73-81.
6. Stroustrup A, Trasande L. Epidemiological characteristics and resource use in neonates with bronchopulmonary dysplasia: 1993-2006. Pediatrics 2010;126:291-297.
7. Doyle LW, Faber B, Callanan C, Freezer N, Ford GW, Davis NM. Bronchopulmonary dysplasia in very low birth weight subjects and lung function in late adolescence. Pediatrics 2006;118:108-113. (Pubitemid 46071153)
8. Shi W, Bellusci S, Warburton D. Lung development and adult lung diseases. Chest 2007;132:651-656. (Pubitemid 47282400)
9. Rehan VK, Sakurai R, Wang Y, Santos J, Huynh K, Torday JS. Reversal of nicotine-induced alveolar lipofibroblast-to-myofibroblast trans-differentiation by stimulants of parathyroid hormone-related protein signaling. Lung 2007;185:151-159. (Pubitemid 46850173)
10. Rehan VK, Wang Y, Patel S, Santos J, Torday JS. Rosiglitazone, a peroxisome proliferator-activated receptor-gamma agonist, prevents hyperoxia-induced neonatal rat lung injury in vivo. Pediatr Pulmonol 2006;41:558-569. (Pubitemid 43801026)
11. Rehan V, Torday J. Hyperoxia augments pulmonary lipofibroblast-to- myofibroblast transdifferentiation. Cell Biochem Biophys 2003;38:239-250.
12. Nicola T, Ambalavanan N, Zhang W, James ML, Rehan V, Halloran B, Olave N, Bulger A, Oparil S, Chen YF. Hypoxia-induced inhibition of lung development is attenuated by the peroxisome proliferator-activated receptor-{gamma} agonist rosiglitazone. Am J Physiol Lung Cell Mol Physiol 2011;301:L125-L134.
13. Ferguson HE, Kulkarni A, Lehmann GM, Garcia-Bates TM, Thatcher TH, Huxlin KR, Phipps RP, Sime PJ. Electrophilic peroxisome proliferator-activated receptor-gamma ligands have potent antifibrotic effects in human lung fibroblasts. Am J Respir Cell Mol Biol 2009;41:722-730.
14. McGowan SE, Jackson SK, Doro MM, Olson PJ. Peroxisome proliferators alter lipid acquisition and elastin gene expression in neonatal rat lung fibroblasts. Am J Physiol 1997;273:L1249-L1257.
15. Dasgupta C, Sakurai R, Wang Y, Guo P, Ambalavanan N, Torday JS, Rehan VK. Hyperoxia-induced neonatal rat lung injury involves activation of TGF-{beta} and WNT signaling and is protected by rosiglitazone. Am J Physiol Lung Cell Mol Physiol 2009;296:L1031-L1041.
16. Torday JS, Torres E, Rehan VK. The role of fibroblast trans-differentiation in lung epithelial cell proliferation, differentiation, and repair in vitro. Pediatr Pathol Mol Med 2003;22:189-207. (Pubitemid 36548148)
17. Sato A, Schehr A, Ikegami M. Leptin does not influence surfactant synthesis in fetal sheep and mice lungs. Am J Physiol Lung Cell Mol Physiol 2011;300:L498-L505.
18. Hagood JS, Prabhakaran P, Kumbla P, Salazar L, MacEwen MW, Barker TH, Ortiz LA, Schoeb T, Siegal GP, Alexander CB, et al. Loss of fibroblast Thy-1 expression correlates with lung fibrogenesis. Am J Pathol 2005;167:365-379. (Pubitemid 43026094)
19. Phipps RP, Baecher C, Frelinger JG, Penney DP, Keng P, Brown D. Differential expression of interleukin 1 alpha by Thy-11 and Thy-12 lung fibroblast subpopulations: enhancement of interleukin 1 alpha production by tumor necrosis factor-alpha. Eur J Immunol 1990;20:1723-1727. (Pubitemid 20290905)
20. McIntosh JC, Hagood JS, Richardson TL, Simecka JW. Thy1 (+) and (-) lung fibrosis subpopulations in LEW and F344 rats. Eur Respir J 1994;7:2131-2138.
21. Phipps RP, Penney DP, Keng P, Quill H, Paxhia A, Derdak S, Felch ME. Characterization of two major populations of lung fibroblasts: distinguishing morphology and discordant display of Thy 1 and Class II MHC. Am J Respir Cell Mol Biol 1989;1:65-74.
22. Zhou Y, Hagood JS, Murphy-Ullrich JE. Thy-1 expression regulates the ability of rat lung fibroblasts to activate transforming growth factor-beta in response to fibrogenic stimuli. Am J Pathol 2004;165:659-669. (Pubitemid 38971395)
23. Sanders YY, Kumbla P, Hagood JS. Enhanced myofibroblastic differentiation and survival in Thy-1(-) lung fibroblasts. Am J Respir Cell Mol Biol 2007;36:226-235. (Pubitemid 46233476)
24. Zhou Y, Hagood JS, Lu B, Merryman WD, Murphy-Ullrich JE. Thy-1-integrin alphaV beta5 interactions inhibit lung fibroblast contraction-induced latent transforming growth factor-beta1 activation and myofibroblast differentiation. J Biol Chem 2010;285:22382-22393.
25. Nicola T, Hagood JS, James ML, Macewen MW, Williams TA, Hewitt MM, Schwiebert L, Bulger A, Oparil S, Chen YF, et al. Loss of Thy-1 inhibits alveolar development in the newborn mouse lung. Am J Physiol Lung Cell Mol Physiol 2009;296:L738-L750.
26. Barker TH, Grenett HE, MacEwen MW, Tilden SG, Fuller GM, Settleman J, Woods A, Murphy-Ullrich J, Hagood JS. Thy-1 regulates fibroblast focal adhesions, cytoskeletal organization and migration through modulation of p190 RhoGAP and rho GTPase activity. Exp Cell Res 2004;295:488-496. (Pubitemid 38490501)
27. Kaplan JM, Cook JA, Hake PW, O'Connor M, Burroughs TJ, Zingarelli B. 15-deoxy-delta(12,14)-prostaglandin J(2) (15D-PGJ(2)), a peroxisome proliferator activated receptor gamma ligand, reduces tissue leukosequestration and mortality in endotoxic shock. Shock 2005;24: 59-65. (Pubitemid 40946596)
28. Besnard V, Wert SE, Stahlman MT, Postle AD, Xu Y, Ikegami M, Whitsett JA. Deletion of SCAP in alveolar Type II cells influences lung lipid homeostasis and identifies a compensatory role for pulmonary lipofibroblasts. J Biol Chem 2009;284:4018-4030.
29. Imamura M, Inoguchi T, Ikuyama S, Taniguchi S, Kobayashi K, Nakashima N, Nawata H. ADRP stimulates lipid accumulation and lipid droplet formation in murine fibroblasts. Am J Physiol Endocrinol Metab 2002;283:E775-E783.
30. Castrillo A, Tontonoz P. Nuclear receptors in macrophage biology: at the crossroads of lipid metabolism and inflammation. Annu Rev Cell Dev Biol 2004;20:455-480. (Pubitemid 39488646)
31. McGowan S, Jackson SK, Jenkins-Moore M, Dai HH, Chambon P, Snyder JM. Mice bearing deletions of retinoic acid receptors demonstrate reduced lung elastin and alveolar numbers. Am J Respir Cell Mol Biol 2000;23:162-167. (Pubitemid 30656424)
32. Hong I, Rho HS, Kim DH, Lee MO. Activation of LXRalpha induces lipogenesis in HACAT cells. Arch Pharm Res 2010;33:1443-1449.
33. McGowan SE, Torday JS. The pulmonary lipofibroblast (lipid interstitial cell) and its contributions to alveolar development. Annu Rev Physiol 1997;59: 43-62. (Pubitemid 27142434)
34. Guthmann F, Haupt R, Looman AC, Spener F, Rustow B. Fatty acid translocase/CD36 mediates the uptake of palmitate by Type II pneumocytes. Am J Physiol 1999;277:L191-L196. (Pubitemid 29356767)
35. Frohnert BI, Hui TY, Bernlohr DA. Identification of a functional peroxisome proliferator-responsive element in the murine fatty acid transport protein gene. J Biol Chem 1999;274:3970-3977.
36. Stahl A. A current review of fatty acid transport proteins (SLC27). Pflugers Arch 2004;447:722-727. (Pubitemid 38241457)
37. Hajri T, Abumrad NA. Fatty acid transport across membranes: relevance to nutrition and metabolic pathology. Annu Rev Nutr 2002;22:383-415. (Pubitemid 35221466)
38. Awonusonu F, Srinivasan S, Strange J, Al-Jumaily W, Bruce MC. Developmental shift in the relative percentages of lung fibroblast subsets: role of apoptosis postseptation. Am J Physiol 1999;277:L848-L859. (Pubitemid 29522653)
39. Tordet C, Marin L, Dameron F. Pulmonary di-and-triacylglycerols during the perinatal development of the rat. Experientia 1981;37: 333-334. (Pubitemid 11108511)
40. Torday J, Hua J, Slavin R. Metabolism and fate of neutral lipids of fetal lung fibroblast origin. Biochim Biophys Acta 1995;1254:198-206.
41. Nunez JS, Torday JS. The developing rat lung fibroblast and alveolar Type II cell actively recruit surfactant phospholipid substrate. J Nutr 1995;125(Suppl. 6)1639S-1644S.
42. Nicola T, Ambalavanan N, Zhang W, James ML, Rehan VK, Halloran BA, Olave N, Bulger A, Oparil S, Chen YF. Hypoxia-induced inhibition of lung development is attenuated by the peroxisome proliferator-activated receptor-{gamma} agonist rosiglitazone. Am J Physiol Lung Cell Mol Physiol 2011;301:L125-L134.
43. Rehan VK, Sakurai R, Corral J, Krebs M, Ibe B, Ihida-Stansbury K, Torday JS. Antenatally administered PPAR-gamma agonist rosiglitazone prevents hyperoxia-induced neonatal rat lung injury. Am J Physiol Lung Cell Mol Physiol 2010;299:L672-L680.
44. Fujino N, Kubo H, Suzuki T, Ota C, Hegab AE, He M, Suzuki S, Yamada M, Kondo T, Kato H, et al. Isolation of alveolar epithelial Type II progenitor cells from adult human lungs. Lab Invest 2011;91: 363-378.
45. Sanders YY, Pardo A, Selman M, Nuovo GJ, Tollefsbol TO, Siegal GP, Hagood JS. Thy-1 promoter hypermethylation: a novel epigenetic pathogenic mechanism in pulmonary fibrosis. Am J Respir Cell Mol Biol 2008;39:610-618.
46. Koumas L, Smith TJ, Feldon S, Blumberg N, Phipps RP. Thy-1 expression in human fibroblast subsets defines myofibroblastic or lipofibroblastic phenotypes. Am J Pathol 2003;163:1291-1300. (Pubitemid 37175078)
47. Khoo TK, Coenen MJ, Schiefer AR, Kumar S, Bahn RS. Evidence for enhanced Thy-1 (CD90) expression in orbital fibroblasts of patients with Graves' ophthalmopathy. Thyroid 2008;18:1291-1296.
48. Lehmann GM, Woeller CF, Pollock SJ, O'Loughlin CW, Gupta S, Feldon SE, Phipps RP. Novel anti-adipogenic activity produced by human fibroblasts. Am J Physiol Cell Physiol 2010;299:C672-C681.