Biomarkers in lung diseases: From pathogenesis to prediction to new therapiescompartment-specific expression of collagens and their processing enzymes in intrapulmonary arteries of IPAH patients

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 10, 2015, Pages L1002-L1013

  Hoffmann, Julia ^a   Marsh, Leigh M ^a   Pieper, Mario ^b   Stacher, Elvira ^a,c   Ghanim, Bahil ^a,d   Kovacs, Gabor ^a,c   König, Peter ^b   Wilkens, Heinrike ^e   Haitchi, Hans Michael ^f,g   Hoefler, Gerald ^c   Klepetko, Walter ^d   Olschewski, Horst ^c   Olschewski, Andrea ^a,c   Kwapiszewska, Grazyna ^a,c  

^a LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^b Institute of Anatomy University Lübeck   (Germany)

^c MEDICAL UNIVERSITY OF GRAZ   (Austria)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e SAARLAND UNIVERSITY   (Germany)

^f UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^g UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Collagen XVIII; Endostatin; Laser microdissection; Vascular fibrosis; Vascular remodeling

Indexed keywords

A DISINTEGRIN AND METALLOPROTEASE 17; A DISINTEGRIN AND METALLOPROTEASE 33; ADAM PROTEIN; AMINO TERMINAL PRO BRAIN NATRIURETIC PEPTIDE; BILIRUBIN; C REACTIVE PROTEIN; COLLAGEN TYPE 11A1; COLLAGEN TYPE 14A1; COLLAGEN TYPE 18; COLLAGEN TYPE 18A1; COLLAGEN TYPE 1A1; COLLAGEN TYPE 1A2; COLLAGEN TYPE 3A1; COLLAGEN TYPE 4A5; COLLAGEN TYPE 5A1; COLLAGEN TYPE 6A3; COLLAGEN TYPE 9A2; ENDOSTATIN; GELATINASE A; INTERSTITIAL COLLAGENASE; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 19; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 3; UNCLASSIFIED DRUG; URIC ACID; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; BIOLOGICAL MARKER; COLLAGEN; METALLOPROTEINASE;

ADULT; ARTERIAL WALL THICKNESS; ARTERY INTIMA; ARTICLE; BILIRUBIN BLOOD LEVEL; CLINICAL ARTICLE; COLLAGEN FIBER; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION PROFILING; HEART INDEX; HEART RIGHT ATRIUM PRESSURE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LASER CAPTURE MICRODISSECTION; MALE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; PULMONARY ARTERY; PULMONARY HYPERTENSION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE DISTRIBUTION; UPREGULATION; URIC ACID BLOOD LEVEL; VASCULAR FIBROSIS; VASCULAR REMODELING; WALKING; BIOSYNTHESIS; BLOOD; GENE EXPRESSION REGULATION; HYPERTENSION, PULMONARY; INTIMA; METABOLISM; MIDDLE AGED; PATHOLOGY;

BIOMARKERS; COLLAGEN; ENDOSTATINS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; HYPERTENSION, PULMONARY; MALE; METALLOPROTEASES; MIDDLE AGED; PROGNOSIS; PULMONARY ARTERY; TUNICA INTIMA;

EID: 84930845309     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00383.2014     Document Type: Article

References (63)

1. Basu R, Fan D, Kandalam V, Lee J, Das SK, Wang X, Baldwin TA, Oudit GY, Kassiri Z. Loss of Timp3 gene leads to abdominal aortic aneurysm formation in response to angiotensin II. J Biol Chem 287: 44083–44096, 2012.
2. Benisty JI, Folkman J, Zurakowski D, Louis G, Rich S, Langleben D, Moses MA. Matrix metalloproteinases in the urine of patients with pulmonary arterial hypertension. Chest 128: 572S, 2005.
3. Berg JT, Breen EC, Fu Z, Mathieu-Costello O, West JB. Alveolar hypoxia increases gene expression of extracellular matrix proteins and platelet-derived growth factor-B in lung parenchyma. Am J Respir Crit Care Med 158: 1920–1928, 1998.
4. Botney MD, Liptay MJ, Kaiser LR, Cooper JD, Parks WC, Mecham RP. Active collagen synthesis by pulmonary arteries in human primary pulmonary hypertension. Am J Pathol 143: 121–129, 1993.
5. Chang JH, Javier JA, Chang GY, Oliveira HB, Azar DT. Functional characterization of neostatins, the MMP-derived, enzymatic cleavage products of type XVIII collagen. FEBS Lett 579: 3601–3606, 2005.
6. Chelladurai P, Seeger W, Pullamsetti SS. Matrix metalloproteinases and their inhibitors in pulmonary hypertension. Eur Respir J 40: 766–782, 2012.
7. Cool CD, Stewart JS, Werahera P, Miller GJ, Williams RL, Voelkel NF, Tuder RM. Three-dimensional reconstruction of pulmonary arteries in plexiform pulmonary hypertension using cell-specific markers. Evidence for a dynamic and heterogeneous process of pulmonary endothelial cell growth. Am J Pathol 155: 411–419, 1999.
8. Cowan KN, Heilbut A, Humpl T, Lam C, Ito S, Rabinovitch M. Complete reversal of fatal pulmonary hypertension in rats by a serine elastase inhibitor. Nat Med 6: 698–702, 2000.
9. Damico R, Kolb TM, Valera L, Wang L, Housten T, Tedford RJ, Kass DA, Rafaels N, Gao L, Barnes KC, Benza RL, Rand JL, Hamid R, Loyd JE, Robbins IM, Hemnes AR, Chung WK, Austin ED, Drum-mond MB, Mathai SC, Hassoun PM. Serum endostatin is a genetically determined predictor of survival in pulmonary arterial hypertension. Am J Respir Crit Care Med 191: 208–218, 2015.
10. Dhanabal M, Ramchandran R, Waterman MJ, Lu H, Knebelmann B, Segal M, Sukhatme VP. Endostatin induces endothelial cell apoptosis. J Biol Chem 274: 11721–11726, 1999.
11. Dijkstra A, Postma DS, Noordhoek JA, Lodewijk ME, Kauffman HF, ten Hacken NH, Timens W. Expression of ADAMs (“a disintegrin and metalloprotease”) in the human lung. Virchows Arch 454: 441–449, 2009.
12. Dodson RB, Morgan M, Galambos C, Hunter KS, Abman SH. Chronic intrauterine pulmonary hypertension increases main pulmonary artery stiffness and adventitial remodeling in fetal sheep. Am J Physiol Lung Cell Mol Physiol 307: L822–L828, 2014.
13. Erickson AC, Couchman JR. Still more complexity in mammalian basement membranes. J Histochem Cytochem 48: 1291–1306, 2000.
14. Erturk A, Becker K, Jahrling N, Mauch CP, Hojer CD, Egen JG, Hellal F, Bradke F, Sheng M, Dodt HU. Three-dimensional imaging of solvent-cleared organs using 3DISCO. Nat Protoc 7: 1983–1995, 2012.
15. Gelse K, Poschl E, Aigner T. Collagens—structure, function, biosynthesis. Adv Drug Deliv Rev 55: 1531–1546, 2003.
16. Gouya G, Siller-Matula JM, Fritzer-Szekeres M, Neuhold S, Storka A, Neuhofer LM, Clodi M, Hulsmann M, Pacher R, Wolzt M. Association of endostatin with mortality in patients with chronic heart failure. Eur J Clin Invest 44: 125–135, 2014.
17. Hayden MR, Sowers JR, Tyagi SC. The central role of vascular extracellular matrix and basement membrane remodeling in metabolic syndrome and type 2 diabetes: the matrix preloaded. Cardiovasc Diabetol 4: 9, 2005.
18. Hendel A, Hsu I, Granville DJ. Granzyme B releases vascular endothe-lial growth factor from extracellular matrix and induces vascular permeability. Lab Invest 94: 716–725, 2014.
19. Heo SH, Choi YJ, Ryoo HM, Cho JY. Expression profiling of ETS and MMP factors in VEGF-activated endothelial cells: role of MMP-10 in VEGF-induced angiogenesis. J Cell Physiol 224: 734–742, 2010.
20. Hoffmann J, Wilhelm J, Marsh LM, Ghanim B, Klepetko W, Kovacs G, Olschewski H, Olschewski A, Kwapiszewska G. Distinct differences in gene expression patterns in pulmonary arteries of patients with chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis with pulmonary hypertension. Am J Respir Crit Care Med 190: 98–111, 2014.
21. Holloway JW, Laxton RC, Rose-Zerilli MJ, Holloway JA, Andrews AL, Riaz Z, Wilson SJ, Simpson IA, Ye S. ADAM33 expression in atherosclerotic lesions and relationship of ADAM33 gene variation with atherosclerosis. Atherosclerosis 211: 224–230, 2010.
22. Jones PL, Cowan KN, Rabinovitch M. Tenascin-C, proliferation and subendothelial fibronectin in progressive pulmonary vascular disease. Am J Pathol 150: 1349–1360, 1997.
23. Jonigk D, Golpon H, Bockmeyer CL, Maegel L, Hoeper MM, Gottlieb J, Nickel N, Hussein K, Maus U, Lehmann U, Janciauskiene S, Welte T, Haverich A, Rische J, Kreipe H, Laenger F. Plexiform lesions in pulmonary arterial hypertension composition, architecture, and microen-vironment. Am J Pathol 179: 167–179, 2011.
24. Kadler KE, Baldock C, Bella J, Boot-Handford RP. Collagens at a glance. J Cell Sci 120: 1955–1958, 2007.
25. Kerr JS, Ruppert CL, Tozzi CA, Neubauer JA, Frankel HM, Yu SY, Riley DJ. Reduction of chronic hypoxic pulmonary hypertension in the rat by an inhibitor of collagen production. Am Rev Respir Dis 135: 300–306, 1987.
26. Kim DH, Kim HS. Serial changes of serum endostatin and angiopoietin-1 levels in preterm infants with severe bronchopulmonary dysplasia and subsequent pulmonary artery hypertension. Neonatology 106: 55–61, 2014.
27. Kim YM, Haghighat L, Spiekerkoetter E, Sawada H, Alvira CM, Wang L, Acharya S, Rodriguez-Colon G, Orton A, Zhao M, Rabin-ovitch M. Neutrophil elastase is produced by pulmonary artery smooth muscle cells and is linked to neointimal lesions. Am J Pathol 179: 1560–1572, 2011.
28. Kwapiszewska G, Markart P, Dahal BK, Kojonazarov B, Marsh LM, Schermuly RT, Taube C, Meinhardt A, Ghofrani HA, Steinhoff M, Seeger W, Preissner KT, Olschewski A, Weissmann N, Wygrecka M. PAR-2 inhibition reverses experimental pulmonary hypertension. Circ Res 110: 1179–1191, 2012.
29. Kwapiszewska G, Wilhelm J, Wolff S, Laumanns I, Koenig IR, Ziegler A, Seeger W, Bohle RM, Weissmann N, Fink L. Expression profiling of laser-microdissected intrapulmonary arteries in hypoxia-in-duced pulmonary hypertension. Respir Res 6: 109, 2005.
30. Lamoreaux WJ, Fitzgerald ME, Reiner A, Hasty KA, Charles ST. Vascular endothelial growth factor increases release of gelatinase A and decreases release of tissue inhibitor of metalloproteinases by microvascu-lar endothelial cells in vitro. Microvasc Res 55: 29–42, 1998.
31. Lepetit H, Eddahibi S, Fadel E, Frisdal E, Munaut C, Noel A, Humbert M, Adnot S, D’Ortho MP, Lafuma C. Smooth muscle cell matrix metalloproteinases in idiopathic pulmonary arterial hypertension. Eur Respir J 25: 834–842, 2005.
32. Mammoto T, Jiang E, Jiang A, Lu Y, Juan AM, Chen J, Mammoto A. Twist1 controls lung vascular permeability and endotoxin-induced pulmonary edema by altering Tie2 expression. PloS One 8: e73407, 2013.
33. Marneros AG, Olsen BR. Physiological role of collagen XVIII and endostatin. FASEB J 19: 716–728, 2005.
34. Matsui K, Takano Y, Yu ZX, Hi JE, Stetler-Stevenson WG, Travis WD, Ferrans VJ. Immunohistochemical study of endothelin-1 and matrix metalloproteinases in plexogenic pulmonary arteriopathy. Pathol Res Pract 198: 403–412, 2002.
35. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, Yuan JX, Weir EK. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 54: S20–S31, 2009.
36. Murphy G. Tissue inhibitors of metalloproteinases. Genome Biol 12: 233, 2011.
37. Nave AH, Mizikova I, Niess G, Steenbock H, Reichenberger F, Tala-vera ML, Veit F, Herold S, Mayer K, Vadasz I, Weissmann N, Seeger W, Brinckmann J, Morty RE. Lysyl oxidases play a causal role in vascular remodeling in clinical and experimental pulmonary arterial hypertension. Arterioscler Thromb Vasc Biol 34: 1446–1458, 2014.
38. Nichols WW. Clinical measurement of arterial stiffness obtained from noninvasive pressure waveforms. Am J Hypertens 18: 3S–10S, 2005.
39. Nicholson R, Murphy G, Breathnach R. Human and rat malignant-tumor-associated mRNAs encode stromelysin-like metalloproteinases. Biochemistry 28: 5195–5203, 1989.
40. Orbe J, Barrenetxe J, Rodriguez JA, Vivien D, Orset C, Parks WC, Birkland TP, Serrano R, Purroy A, Martinez de Lizarrondo S, Angles-Cano E, Paramo JA. Matrix metalloproteinase-10 effectively reduces infarct size in experimental stroke by enhancing fibrinolysis via a thrombin-activatable fibrinolysis inhibitor-mediated mechanism. Circulation 124: 2909–2919, 2011.
41. Paulissen G, Rocks N, Gueders MM, Crahay C, Quesada-Calvo F, Bekaert S, Hacha J, El Hour M, Foidart JM, Noel A, Cataldo DD. Role of ADAM and ADAMTS metalloproteinases in airway diseases. Respir Res 10: 127, 2009.
42. Pietra GG, Edwards WD, Kay JM, Rich S, Kernis J, Schloo B, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, Fishman AP, GOldring RM, Groves BM, Levy PS, Reid LM, Vreim CE, Williams GW. Histopathology of primary pulmonary hypertension. A qualitative and quantitative study of pulmonary blood vessels from 58 patients in the National Heart, Lung, and Blood Institute, Primary Pulmonary Hypertension Registry. Circulation 80: 1198–1206, 1989.
43. Poiani GJ, Tozzi CA, Yohn SE, Pierce RA, Belsky SA, Berg RA, Yu SY, Deak SB, Riley DJ. Collagen and elastin metabolism in hypertensive pulmonary arteries of rats. Circ Res 66: 968–978, 1990.
44. Price LC, Wort SJ, Perros F, Dorfmuller P, Huertas A, Montani D, Cohen-Kaminsky S, Humbert M. Inflammation in pulmonary arterial hypertension. Chest 141: 210–221, 2012.
45. Puxeddu I, Pang YY, Harvey A, Haitchi HM, Nicholas B, Yoshisue H, Ribatti D, Clough G, Powell RM, Murphy G, Hanley NA, Wilson DI, Howarth PH, Holgate ST, Davies DE. The soluble form of a disintegrin and metalloprotease 33 promotes angiogenesis: implications for airway remodeling in asthma. J Allergy Clin Immunol 121: 1400–1406, 1406.e1– e4, 2008.
46. Rabinovitch M. Pathobiology of pulmonary hypertension. Extracellular matrix. Clin Chest Med 22: 433–449, 8, 2001.
47. Rehn M, Veikkola T, Kukk-Valdre E, Nakamura H, Ilmonen M, Lombardo C, Pihlajaniemi T, Alitalo K, Vuori K. Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci USA 98: 1024–1029, 2001.
48. Rong B, Yang S, Li W, Zhang W, Ming Z. Systematic review and meta-analysis of Endostar (rh-endostatin) combined with chemotherapy versus chemotherapy alone for treating advanced non-small cell lung cancer. World J Surg Oncol 10: 170, 2012.
49. Rubin LJ. Primary pulmonary hypertension. N Engl J Med 336: 111–117, 1997.
50. Saarela J, Rehn M, Oikarinen A, Autio-Harmainen H, Pihlajaniemi T. The short and long forms of type XVIII collagen show clear tissue specificities in their expression and location in basement membrane zones in humans. Am J Pathol 153: 611–626, 1998.
51. Safdar Z, Tamez E, Chan W, Arya B, Ge Y, Deswal A, Bozkurt B, Frost A, Entman M. Circulating collagen biomarkers as indicators of disease severity in pulmonary arterial hypertension. JACC Heart Fail 2: 412–421, 2014.
52. Schumann C, Lepper PM, Frank H, Schneiderbauer R, Wibmer T, Kropf C, Stoiber KM, Rudiger S, Kruska L, Krahn T, Kramer F. Circulating biomarkers of tissue remodelling in pulmonary hypertension. Biomarkers 15: 523–532, 2010.
53. Shimoda LA, Laurie SS. Vascular remodeling in pulmonary hypertension. J Mol Med 91: 297–309, 2013.
54. Simonneau G, Gatzoulis MA, Adatia I, Celermajer D, Denton C, Ghofrani A, Gomez Sanchez MA, Krishna Kumar R, Landzberg M, Machado RF, Olschewski H, Robbins IM, Souza R. Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol 62: D34–D41, 2013.
55. Skovseth DK, Veuger MJ, Sorensen DR, De Angelis PM, Haraldsen G. Endostatin dramatically inhibits endothelial cell migration, vascular morphogenesis, and perivascular cell recruitment in vivo. Blood 105: 1044–1051, 2005.
56. Stacher E, Graham BB, Hunt JM, Gandjeva A, Groshong SD, McLaughlin VV, Jessup M, Grizzle WE, Aldred MA, Cool CD, Tuder RM. Modern age pathology of pulmonary arterial hypertension. Am J Respir Crit Care Med 186: 261–272, 2012.
57. Todorovich-Hunter L, Dodo H, Ye C, McCready L, Keeley FW, Rabinovitch M. Increased pulmonary artery elastolytic activity in adult rats with monocrotaline-induced progressive hypertensive pulmonary vascular disease compared with infant rats with nonprogressive disease. Am Rev Respir Dis 146: 213–223, 1992.
58. Tuder RM, Archer SL, Dorfmuller P, Erzurum SC, Guignabert C, Michelakis E, Rabinovitch M, Schermuly R, Stenmark KR, Morrell NW. Relevant issues in the pathology and pathobiology of pulmonary hypertension. J Am Coll Cardiol 62: D4–D12, 2013.
59. Tuder RM, Chacon M, Alger L, Wang J, Taraseviciene-Stewart L, Kasahara Y, Cool CD, Bishop AE, Geraci M, Semenza GL, Yacoub M, Polak JM, Voelkel NF. Expression of angiogenesis-related molecules in plexiform lesions in severe pulmonary hypertension: evidence for a process of disordered angiogenesis. J Pathol 195: 367–374, 2001.
60. Uzui H, Lee JD, Shimizu H, Tsutani H, Ueda T. The role of protein-tyrosine phosphorylation and gelatinase production in the migration and proliferation of smooth muscle cells. Atherosclerosis 149: 51–59, 2000.
61. Wagenseil JE, Mecham RP. Vascular extracellular matrix and arterial mechanics. Physiol Rev 89: 957–989, 2009.
62. Wang Z, Lakes RS, Eickhoff JC, Chesler NC. Effects of collagen deposition on passive and active mechanical properties of large pulmonary arteries in hypoxic pulmonary hypertension. Biomech Model Mechanobiol 12: 1115–1125, 2013
63. Yu G, Kovkarova-Naumovski E, Jara P, Parwani A, Kass D, Ruiz V, Lopez-Otin C, Rosas IO, Gibson KF, Cabrera S, Ramirez R, Yousem SA, Richards TJ, Chensny LJ, Selman M, Kaminski N, Pardo A. Matrix metalloproteinase-19 is a key regulator of lung fibrosis in mice and humans. Am J Respir Crit Care Med 186: 752–762, 2012.