Decreased laminin expression by human lung epithelial cells and fibroblasts cultured in acellular lung scaffolds from aged mice

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Godin, Lindsay M ^a,c   Sandri, Brian J ^a   Wagner, Darcy E ^b   Meyer, Carolyn M ^a   Price, Andrew P ^a   Akinnola, Ifeolu ^a   Weiss, Daniel J ^b   Panoskaltsis Mortari, Angela Panoskaltsis Mortari ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^c Boston Scientific   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; ELASTIN; FIBRONECTIN; LAMININ; LAMININ ALPHA3; LAMININ ALPHA4; UNCLASSIFIED DRUG; CADHERIN; LAMININ ALPHA 3; SCLEROPROTEIN; THROMBOPLASTIN;

AGED; AGING; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST CULTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; LAMININ ALPHA3 GENE; LAMININ ALPHA4 GENE; LUNG ALVEOLUS EPITHELIUM CELL; LUNG FIBROBLAST; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; TISSUE SCAFFOLD; AGE; ANIMAL; CELL CULTURE TECHNIQUE; FIBROBLAST; GENE EXPRESSION PROFILING; GENETICS; LUNG; METABOLISM; PATHOLOGY; PHENOTYPE;

AGE FACTORS; ALVEOLAR EPITHELIAL CELLS; ANIMALS; CADHERINS; CELL CULTURE TECHNIQUES; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION PROFILING; LAMININ; LUNG; MALE; MICE; PHENOTYPE; THROMBOPLASTIN;

EID: 84961159953     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0150966     Document Type: Article

References (55)

1. Meiners S, Eickelberg O, Konigshoff M. Hallmarks of the ageing lung. Eur Respir J. 2015; 45(3):807-27. Epub 2015/02/07. doi: 10.1183/09031936.00186914 09031936.00186914 [pii]. PMID: 25657021.
2. Kent S. The aging lung. Part 1. Loss of elasticity. Geriatrics. 1978; 33(2):124-32. Epub 1978/02/01. PMID: 340344.
3. Thannickal VJ, Murthy M, Balch WE, Chandel NS, Meiners S, Eickelberg O, et al. Blue journal conference. Aging and susceptibility to lung disease. Am J Respir Crit Care Med. 2015; 191(3):261-9. Epub 2015/01/16. doi: 10.1164/rccm.201410-1876PP PMID: 25590812; PubMed Central PMCID: PMC4351581.
4. Huang K, Rabold R, Schofield B, Mitzner W, Tankersley CG. Age-dependent changes of airway and lung parenchyma in C57BL/6J mice. J Appl Physiol (1985). 2007; 102(1):200-6. Epub 2006/09/02. 00400.2006 [pii] doi: 10.1152/japplphysiol.00400.2006 PMID: 16946023.
5. D'Errico A, Scarani P, Colosimo E, Spina M, Grigioni WF, Mancini AM. Changes in the alveolar connective tissue of the ageing lung. An immunohistochemical study. Virchows Arch A Pathol Anat Histopathol. 1989; 415(2):137-44. Epub 1989/01/01. PMID: 2500769.
6. Fulop T Jr, Douziech N, Jacob MP, Hauck M, Wallach J, Robert L. Age-related alterations in the signal transduction pathways of the elastin-laminin receptor. Pathol Biol (Paris). 2001; 49(4):339-48. Epub 2001/06/29. S0369-8114(01)00143-2 [pii]. PMID: 11428170.
7. Sueblinvong V, Neujahr DC, Mills ST, Roser-Page S, Ritzenthaler JD, Guidot D, et al. Predisposition for disrepair in the aged lung. Am J Med Sci. 2012; 344(1):41-51. Epub 2011/12/17. doi: 10.1097/MAJ. 0b013e318234c132 PMID: 22173045; PubMed Central PMCID: PMC3395069.
8. Kulkarni T, O'Reilly P, Antony VB, Gaggar A, Thannickal VJ. Matrix Remodeling in Pulmonary Fibrosis and Emphysema. Am J Respir Cell Mol Biol. 2016. Epub 2016/01/08. doi: 10.1165/rcmb.2015-0166PS PMID: 26741177.
9. Sokocevic D, Bonenfant NR, Wagner DE, Borg ZD, Lathrop MJ, Lam YW, et al. The effect of age and emphysematous and fibrotic injury on the re-cellularization of de-cellularized lungs. Biomaterials. 2013; 34(13):3256-69. Epub 2013/02/07. S0142-9612(13)00044-6 [pii] doi: 10.1016/j.biomaterials.2013.01. 028 PMID: 23384794.
10. Price AP, England KA, Matson AM, Blazar BR, Panoskaltsis-Mortari A. Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. Tissue Eng Part A. 2010; 16(8):2581-91. Epub 2010/03/20. doi: 10.1089/ten.TEA.2009.0659 PMID: 20297903; PubMed Central PMCID: PMC2947435.
11. Xia H, Bodempudi V, Benyumov A, Hergert P, Tank D, Herrera J, et al. Identification of a cell-of-origin for fibroblasts comprising the fibrotic reticulum in idiopathic pulmonary fibrosis. Am J Pathol. 2014; 184 (5):1369-83. Epub 2014/03/19. doi: 10.1016/j.ajpath.2014.01.012 S0002-9440(14)00085-6 [pii]. PMID: 24631025; PubMed Central PMCID: PMC4005984.
12. Barbosa I, Garcia S, Barbier-Chassefiere V, Caruelle JP, Martelly I, Papy-Garcia D. Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology. 2003; 13(9):647-53. PMID: 12773478.
13. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics. 2004; 3(12):1154-69. Epub 2004/09/24. doi: 10.1074/mcp.M400129-MCP200 M400129-MCP200 [pii]. PMID: 15385600.
14. Calvi CL, Podowski M, D'Alessio FR, Metzger SL, Misono K, Poonyagariyagorn H, et al. Critical transition in tissue homeostasis accompanies murine lung senescence. PLoS One. 2011; 6(6):e20712. Epub 2011/06/30. doi: 10.1371/journal.pone.0020712 PONE-D-11-00109 [pii]. PMID: 21713037; PubMed Central PMCID: PMC3119663.
15. Nguyen NM, Senior RM. Laminin isoforms and lung development: all isoforms are not equal. Dev Biol. 2006; 294(2):271-9. Epub 2006/04/29. S0012-1606(06)00235-1 [pii] doi: 10.1016/j.ydbio.2006.03.032 PMID: 16643883.
16. Iivanainen A, Kortesmaa J, Sahlberg C, Morita T, Bergmann U, Thesleff I, et al. Primary structure, developmental expression, and immunolocalization of the murine laminin alpha4 chain. J Biol Chem. 1997; 272(44):27862-8. Epub 1997/11/05. PMID: 9346933.
17. Urich D, Eisenberg JL, Hamill KJ, Takawira D, Chiarella SE, Soberanes S, et al. Lung-specific loss of the laminin alpha3 subunit confers resistance to mechanical injury. J Cell Sci. 2011; 124(Pt 17):2927-37. Epub 2011/09/01. 124/17/2927 [pii] doi: 10.1242/jcs.080911 PMID: 21878500; PubMed Central PMCID: PMC3166037.
18. Kligys K, Wu Y, Hamill KJ, Lewandowski KT, Hopkinson SB, Budinger GR, et al. Laminin-332 and alpha3beta1 integrin-supported migration of bronchial epithelial cells is modulated by fibronectin. Am J Respir Cell Mol Biol. 2013; 49(5):731-40. Epub 2013/04/18. doi: 10.1165/rcmb.2012-0509OC PMID: 23590307.
19. Booth AJ, Hadley R, Cornett AM, Dreffs AA, Matthes SA, Tsui JL, et al. Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. Am J Respir Crit Care Med. 2012; 186(9):866-76. Epub 2012/09/01. rccm.201204-0754OC [pii] doi: 10.1164/rccm.201204-0754OC PMID: 22936357; PubMed Central PMCID: PMC3530219.
20. Yousif LF, Di Russo J, Sorokin L. Laminin isoforms in endothelial and perivascular basement membranes. Cell Adh Migr. 2013; 7(1):101-10. Epub 2012/12/25. 22680 [pii] doi: 10.4161/cam.22680 PMID: 23263631; PubMed Central PMCID: PMC3544773.
21. Abrass CK, Hansen KM, Patton BL. Laminin alpha4-null mutant mice develop chronic kidney disease with persistent overexpression of platelet-derived growth factor. Am J Pathol. 2010; 176(2):839-49. Epub 2009/12/26. S0002-9440(10)60396-3 [pii] doi: 10.2353/ajpath.2010.090570 PMID: 20035058; PubMed Central PMCID: PMC2808089.
22. Hagood JS, Prabhakaran P, Kumbla P, Salazar L, MacEwen MW, Barker TH, et al. Loss of fibroblast Thy-1 expression correlates with lung fibrogenesis. Am J Pathol. 2005; 167(2):365-79. Epub 2005/07/29. S0002-9440(10)62982-3 [pii] doi: 10.1016/S0002-9440(10)62982-3 PMID: 16049324; PubMed Central PMCID: PMC1603564.
23. Sueblinvong V, Neveu WA, Neujahr DC, Mills ST, Rojas M, Roman J, et al. Aging promotes pro-fibrotic matrix production and increases fibrocyte recruitment during acute lung injury. Adv Biosci Biotechnol. 2014; 5(1):19-30. Epub 2014/03/07. doi: 10.4236/abb.2014.51004 PMID: 24596659; PubMed Central PMCID: PMC3939026.
24. Parker MW, Rossi D, Peterson M, Smith K, Sikstrom K, White ES, et al. Fibrotic extracellular matrix activates a profibrotic positive feedback loop. J Clin Invest. 2014; 124(4):1622-35. Epub 2014/03/05. doi: 10.1172/JCI71386 71386 [pii]. PMID: 24590289; PubMed Central PMCID: PMC3971953.
25. Bianchi-Frias D, Vakar-Lopez F, Coleman IM, Plymate SR, Reed MJ, Nelson PS. The effects of aging on the molecular and cellular composition of the prostate microenvironment. PLoS One. 2010; 5(9). Epub 2010/09/09. doi: 10.1371/journal.pone.0012501 e12501 [pii]. PMID: 20824135; PubMed Central PMCID: PMC2931699.
26. Seyer JM, Hutcheson ET, Kang AH. Collagen polymorphism in idiopathic chronic pulmonary fibrosis. J Clin Invest. 1976; 57(6):1498-507. Epub 1976/06/01. doi: 10.1172/JCI108420 PMID: 777026; PubMed Central PMCID: PMC436809.
27. Jugdutt BI. Remodeling of the myocardium and potential targets in the collagen degradation and synthesis pathways. Curr Drug Targets Cardiovasc Haematol Disord. 2003; 3(1):1-30. Epub 2003/05/29. PMID: 12769643.
28. Clark RA, Nielsen LD, Welch MP, McPherson JM. Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-beta. J Cell Sci. 1995; 108 (Pt 3):1251-61. Epub 1995/03/01. PMID: 7622608.
29. Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, et al. Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem. 2000; 275(50):39027-31. Epub 2000/ 09/08. doi: 10.1074/jbc.M006700200 M006700200 [pii]. PMID: 10976109.
30. Mays PK, McAnulty RJ, Laurent GJ. Age-related changes in lung collagen metabolism. A role for degradation in regulating lung collagen production. Am Rev Respir Dis. 1989; 140(2):410-6. Epub 1989/08/ 01. doi: 10.1164/ajrccm/140.2.410 PMID: 2788379.
31. Damodarasamy M, Vernon RB, Chan CK, Plymate SR, Wight TN, Reed MJ. Hyaluronan in aged collagen matrix increases prostate epithelial cell proliferation. In Vitro Cell Dev Biol Anim. 2014. Epub 2014/ 08/16. doi: 10.1007/s11626-014-9800-z PMID: 25124870.
32. Neill T, Schaefer L, Iozzo RV. Decorin: a guardian from the matrix. Am J Pathol. 2012; 181(2):380-7. Epub 2012/06/28. doi: 10.1016/j.ajpath.2012.04.029 S0002-9440(12)00414-2 [pii]. PMID: 22735579; PubMed Central PMCID: PMC3409438.
33. Nastase MV, Iozzo RV, Schaefer L. Key roles for the small leucine-rich proteoglycans in renal and pulmonary pathophysiology. Biochim Biophys Acta. 2014; 1840(8):2460-70. Epub 2014/02/11. doi: 10. 1016/j.bbagen.2014.01.035 S0304-4165(14)00046-4 [pii]. PMID: 24508120; PubMed Central PMCID: PMC4074572.
34. Kielty CM, Baldock C, Lee D, Rock MJ, Ashworth JL, Shuttleworth CA. Fibrillin: from microfibril assembly to biomechanical function. Philos Trans R Soc Lond B Biol Sci. 2002; 357(1418):207-17. Epub 2002/03/26. doi: 10.1098/rstb.2001.1029 PMID: 11911778; PubMed Central PMCID: PMC1692929.
35. Sherratt MJ. Age-Related Tissue Stiffening: Cause and Effect. Adv Wound Care (New Rochelle). 2013; 2(1):11-7. Epub 2014/02/15. doi: 10.1089/wound.2011.0328 [pii]. PMID: 24527318; PubMed Central PMCID: PMC3840474.
36. Zanetti M, Braghetta P, Sabatelli P, Mura I, Doliana R, Colombatti A, et al. EMILIN-1 deficiency induces elastogenesis and vascular cell defects. Mol Cell Biol. 2004; 24(2):638-50. Epub 2004/01/01. PMID: 14701737; PubMed Central PMCID: PMC343785.
37. Zacchigna L, Vecchione C, Notte A, Cordenonsi M, Dupont S, Maretto S, et al. Emilin1 links TGF-beta maturation to blood pressure homeostasis. Cell. 2006; 124(5):929-42. Epub 2006/03/15. S0092-8674 (06)00114-0 [pii] doi: 10.1016/j.cell.2005.12.035 PMID: 16530041.
38. Schiller HB, Fernandez IE, Burgstaller G, Schaab C, Scheltema RA, Schwarzmayr T, et al. Time- and compartment-resolved proteome profiling of the extracellular niche in lung injury and repair. Mol Syst Biol. 2015; 11(7):819. Epub 2015/07/16. doi: 10.15252/msb.20156123 PMID: 26174933; PubMed Central PMCID: PMC4547847.
39. Hill RC, Calle EA, Dzieciatkowska M, Niklason LE, Hansen KC. Quantification of extracellular matrix proteins from a rat lung scaffold to provide a molecular readout for tissue engineering. Mol Cell Proteomics. 2015; 14(4):961-73. Epub 2015/02/11. doi: 10.1074/mcp.M114.045260 M114.045260 [pii]. PMID: 25660013; PubMed Central PMCID: PMC4390273.
40. Sicari BM, Johnson SA, Siu BF, Crapo PM, Daly KA, Jiang H, et al. The effect of source animal age upon the in vivo remodeling characteristics of an extracellular matrix scaffold. Biomaterials. 2012; 33 (22):5524-33. Epub 2012/05/12. S0142-9612(12)00439-5 [pii] doi: 10.1016/j.biomaterials.2012.04.017 PMID: 22575834; PubMed Central PMCID: PMC3569720.
41. Nakayama KH, Batchelder CA, Lee CI, Tarantal AF. Renal tissue engineering with decellularized rhesus monkey kidneys: age-related differences. Tissue Eng Part A. 2011; 17(23-24):2891-901. Epub 2011/09/10. doi: 10.1089/ten.TEA.2010.0714 PMID: 21902603; PubMed Central PMCID: PMC3226054.
42. Lynch K, Pei M. Age associated communication between cells and matrix: a potential impact on stem cell-based tissue regeneration strategies. Organogenesis. 2014; 10(3):289-98. Epub 2014/12/09. doi: 10.4161/15476278.2014.970089 PMID: 25482504; PubMed Central PMCID: PMC4594597.
43. Osakabe T, Hayashi M, Hasegawa K, Okuaki T, Ritty TM, Mecham RP, et al. Age- and gender-related changes in ligament components. Ann Clin Biochem. 2001; 38(Pt 5):527-32. Epub 2001/10/06. PMID: 11587131.
44. Komosinska-Vassev K, Olczyk P, Winsz-Szczotka K, Kuznik-Trocha K, Klimek K, Olczyk K. Age- and gender-dependent changes in connective tissue remodeling: physiological differences in circulating MMP-3, MMP-10, TIMP-1 and TIMP-2 level. Gerontology. 2011; 57(1):44-52. Epub 2010/03/11. doi: 10.1159/000295775 000295775 [pii]. PMID: 20215736.
45. Olafsdottir IS, Janson C, Lind L, Hulthe J, Gunnbjornsdottir M, Sundstrom J. Serum levels of matrix metalloproteinase-9, tissue inhibitors of metalloproteinase-1 and their ratio are associated with impaired lung function in the elderly: a population-based study. Respirology. 2010; 15(3):530-5. Epub 2010/03/27. doi: 10.1111/j.1440-1843.2010.01718.x RES1718 [pii]. PMID: 20337997.
46. Dworatzek E, Baczko I, Kararigas G. Effects of aging on cardiac extracellular matrix in men and women. Proteomics Clin Appl. 2016; 10(1):84-91. Epub 2015/08/19. doi: 10.1002/prca.201500031 PMID: 26280680.
47. Carey MA, Card JW, Voltz JW, Arbes SJ Jr, Germolec DR, Korach KS, et al. It's all about sex: gender, lung development and lung disease. Trends Endocrinol Metab. 2007; 18(8):308-13. Epub 2007/09/04. S1043-2760(07)00132-4 [pii] doi: 10.1016/j.tem.2007.08.003 PMID: 17764971; PubMed Central PMCID: PMC2391086.
48. McGee SP, Zhang H, Karmaus W, Sabo-Attwood T. Influence of sex and disease severity on gene expression profiles in individuals with idiopathic pulmonary fibrosis. Int J Mol Epidemiol Genet. 2014; 5 (2):71-86. Epub 2014/06/25. PMID: 24959312; PubMed Central PMCID: PMC4065396.
49. Gharaee-Kermani M, Hatano K, Nozaki Y, Phan SH. Gender-based differences in bleomycin-induced pulmonary fibrosis. Am J Pathol. 2005; 166(6):1593-606. Epub 2005/05/28. S0002-9440(10)62470-4 [pii] doi: 10.1016/S0002-9440(10)62470-4 PMID: 15920145; PubMed Central PMCID: PMC1602429.
50. Haston CK, Wang M, Dejournett RE, Zhou X, Ni D, Gu X, et al. Bleomycin hydrolase and a genetic locus within the MHC affect risk for pulmonary fibrosis in mice. Hum Mol Genet. 2002; 11(16):1855-63. Epub 2002/07/26. PMID: 12140188.
51. Lekgabe ED, Royce SG, Hewitson TD, Tang ML, Zhao C, Moore XL, et al. The effects of relaxin and estrogen deficiency on collagen deposition and hypertrophy of nonreproductive organs. Endocrinology. 2006; 147(12):5575-83. Epub 2006/08/29. en.2006-0533 [pii] doi: 10.1210/en.2006-0533 PMID: 16935837.
52. Voltz JW, Card JW, Carey MA, Degraff LM, Ferguson CD, Flake GP, et al. Male sex hormones exacerbate lung function impairment after bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol. 2008; 39(1):45-52. Epub 2008/02/16. doi: 10.1165/rcmb.2007-0340OC 2007-0340OC [pii]. PMID: 18276795; PubMed Central PMCID: PMC2438447.
53. Groves AM, Gow AJ, Massa CB, Hall L, Laskin JD, Laskin DL. Age-related increases in ozone-induced injury and altered pulmonary mechanics in mice with progressive lung inflammation. Am J Physiol Lung Cell Mol Physiol. 2013; 305(8):L555-68. Epub 2013/09/03. doi: 10.1152/ajplung.00027.2013 ajplung00027.2013 [pii]. PMID: 23997172; PubMed Central PMCID: PMC3798776.
54. Melo E, Cardenes N, Garreta E, Luque T, Rojas M, Navajas D, et al. Inhomogeneity of local stiffness in the extracellular matrix scaffold of fibrotic mouse lungs. J Mech Behav Biomed Mater. 2014; 37:186-95. Epub 2014/06/20. doi: 10.1016/j.jmbbm.2014.05.019 S1751-6161(14)00152-0 [pii]. PMID: 24946269.
55. Lin YM, Zhang A, Rippon HJ, Bismarck A, Bishop AE. Tissue engineering of lung: the effect of extracellular matrix on the differentiation of embryonic stem cells to pneumocytes. Tissue Eng Part A. 2010; 16 (5):1515-26. Epub 2009/12/17. doi: 10.1089/ten.TEA.2009.0232 PMID: 20001250.