Sustained effects of sirolimus on lung function and cystic lung lesions in lymphangioleiomyomatosis

American Journal of Respiratory and Critical Care Medicine

Volumn 190, Issue 11, 2014, Pages 1273-1282

  Yao, Jianhua ^a   Taveira DaSilva, Angelo M ^b   Jones, Amanda M ^b   Julien Williams, Patricia ^b   Stylianou, Mario ^b   Moss, Joel ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

LAM; Lung cystic destruction; Sirolimus

Indexed keywords

ANTINEOPLASTIC ANTIBIOTIC; RAPAMYCIN;

ADULT; COMPUTER ASSISTED TOMOGRAPHY; CYSTS; DISEASE COURSE; DRUG EFFECTS; FORCED EXPIRATORY VOLUME; HUMAN; LUNG; LUNG FUNCTION TEST; LUNG NEOPLASMS; LYMPHANGIOLEIOMYOMATOSIS; PATHOLOGY; PATHOPHYSIOLOGY; QUALITY OF LIFE; RADIOGRAPHY; TIME;

ADULT; ANTIBIOTICS, ANTINEOPLASTIC; CYSTS; DISEASE PROGRESSION; FORCED EXPIRATORY VOLUME; HUMANS; LUNG; LUNG NEOPLASMS; LYMPHANGIOLEIOMYOMATOSIS; QUALITY OF LIFE; RESPIRATORY FUNCTION TESTS; SIROLIMUS; TIME FACTORS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84916226614     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201405-0918OC     Document Type: Article

References (47)

1. Ryu JH, Moss J, Beck GJ, Lee JC, Brown KK, Chapman JT, Finlay GA, Olson EJ, Ruoss SJ, Maurer JR, et al.; NHLBI LAM Registry Group. The NHLBI lymphangioleiomyomatosis registry: characteristics of 230 patients at enrollment. Am J Respir Crit Care Med 2006;173:105-111.
2. McCormack FX. Lymphangioleiomyomatosis: a clinical update. Chest 2008;133:507-516.
3. Meraj R, Wikenheiser-Brokamp KA, Young LR, McCormack FX. Lymphangioleiomyomatosis: new concepts in pathogenesis, diagnosis, and treatment. Semin Respir Crit Care Med 2012;33:486-497.
4. Ferrans VJ, Yu ZX, Nelson WK, Valencia JC, Tatsuguchi A, Avila NA, Riemenschn W, Matsui K, Travis WD, Moss J. Lymphangioleiomyomatosis (LAM): a review of clinical and morphological features. J Nippon Med Sch 2000;67:311-329.
5. Oprescu N, McCormack FX, Byrnes S, Kinder BW. Clinical predictors of mortality and cause of death in lymphangioleiomyomatosis: a population-based registry. Lung 2013;191:35-42.
6. Yu J, Astrinidis A, Henske EP. Chromosome 16 loss of heterozygosity in tuberous sclerosis and sporadic lymphangiomyomatosis. Am J Respir Crit Care Med 2001;164:1537-1540.
7. Smolarek TA, Wessner LL, McCormack FX, Mylet JC, Menon AG, Henske EP. Evidence that lymphangiomyomatosis is caused by TSC2 mutations: chromosome 16p13 loss of heterozygosity in angiomyolipomas and lymph nodes from women with lymphangiomyomatosis. Am J Hum Genet 1998;62:810-815.
8. Carsillo T, Astrinidis A, Henske EP. Mutations in the tuberous sclerosis complex gene TSC2 are a cause of sporadic pulmonary lymphangioleiomyomatosis. Proc Natl Acad Sci USA 2000;97:6085-6090.
9. Rosner M, Hanneder M, Siegel N, Valli A, Hengstschläger M. The tuberous sclerosis gene products hamartin and tuberin are multifunctional proteins with a wide spectrum of interacting partners. Mutat Res 2008;658:234-246.
10. Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 2010;40:310-322.
11. Yuan HX, Xiong Y, Guan KL. Nutrient sensing, metabolism, and cell growth control. Mol Cell 2013;49:379-387.
12. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 2003;13:1259-1268.
13. Krymskaya VP, Goncharova EA. PI3K/mTORC1 activation in hamartoma syndromes: therapeutic prospects. Cell Cycle 2009;8:403-413.
14. Castro AF, Rebhun JF, Clark GJ, Quilliam LA. Rheb binds tuberous sclerosis complex 2 (TSC2) and promotes S6 kinase activation in a rapamycin- and farnesylation-dependent manner. J Biol Chem 2003;278:32493-32496.
15. Bissler JJ, McCormack FX, Young LR, Elwing JM, Chuck G, Leonard JM, Schmithorst VJ, Laor T, Brody AS, Bean J, et al. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N Engl J Med 2008;358:140-151.
16. Dabora SL, Franz DN, Ashwal S, Sagalowsky A, DiMario FJ Jr, Miles D, Cutler D, Krueger D, Uppot RN, Rabenou R, et al. Multicenter phase 2 trial of sirolimus for tuberous sclerosis: kidney angiomyolipomas and other tumors regress and VEGF- D levels decrease. PLoS ONE 2011;6:e23379.
17. Bissler JJ, Kingswood JC, Radzikowska E, Zonnenberg BA, Frost M, Belousova E, Sauter M, Nonomura N, Brakemeier S, de Vries PJ, et al. Everolimus for angiomyolipoma associated with tuberous sclerosis complex or sporadic lymphangioleiomyomatosis (EXIST-2): a multicentre, randomised, double-blind, placebo-controlled trial. Lancet 2013;381:817-824.
18. Krueger DA, Care MM, Holland K, Agricola K, Tudor C, Mangeshkar P, Wilson KA, Byars A, Sahmoud T, Franz DN. Everolimus for subependymal giant-cell astrocytomas in tuberous sclerosis. N Engl J Med 2010;363:1801-1811.
19. Franz DN, Belousova E, Sparagana S, Bebin EM, Frost M, Kuperman R, Witt O, Kohrman MH, Flamini JR, Wu JY, et al. Efficacy and safety of everolimus for subependymal giant cell astrocytomas associated with tuberous sclerosis complex (EXIST-1): a multicentre, randomised, placebo-controlled phase 3 trial. Lancet 2013;381:125-132.
20. Tanaka M, Wataya-Kaneda M, Nakamura A, Matsumoto S, Katayama I. First left-right comparative study of topical rapamycin vs. vehicle for facial angiofibromas in patients with tuberous sclerosis complex. Br J Dermatol 2013;169:1314-1318.
21. McCormack FX, Inoue Y, Moss J, Singer LG, Strange C, Nakata K, Barker AF, Chapman JT, Brantly ML, Stocks JM, et al.; National Institutes of Health Rare Lung Diseases Consortium; MILES Trial Group. Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N Engl J Med 2011;364:1595-1606.
22. Taveira-DaSilva AM, Hathaway O, Stylianou M, Moss J. Changes in lung function and chylous effusions in patients with lymphangioleiomyomatosis treated with sirolimus. Ann Intern Med 2011;154:797-805, W-292-W-293.
23. Moua T, Olson EJ, Jean HC, Ryu JH. Resolution of chylous pulmonary congestion and respiratory failure in lymphangioleiomyomatosis with sirolimus therapy. Am J Respir Crit Care Med 2012;186:389-390.
24. Yao J, Taveira-DaSilva AM, Colby TV, Moss J. Computed tomography grading of lung disease in lymphangioleiomyomatosis. AJR Am J Roentgenol 2012;199:787-793.
25. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CPM, Gustafsson P, et al.; ATS/ERS Task Force. Standardisation of spirometry. Eur Respir J 2005;26:319-338.
26. Macintyre N, Crapo RO, Viegi G, Johnson DC, van der Grinten CPM, Brusasco V, Burgos F, Casaburi R, Coates A, Enright P, et al. Standardisation of the single-breath determination of carbon monoxide uptake in the lung. Eur Respir J 2005;26:720-735.
27. Taveira-DaSilva AM, Stylianou MP, Hedin CJ, Hathaway O, Moss J. Decline in lung function in patients with lymphangioleiomyomatosis treated with or without progesterone. Chest 2004;126:1867-1874.
28. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med 2002;166:111-117.
29. Taveira-DaSilva AM, Stylianou MP, Hedin CJ, Kristof AS, Avila NA, Rabel A, Travis WD, Moss J. Maximal oxygen uptake and severity of disease in lymphangioleiomyomatosis. Am J Respir Crit Care Med 2003;168:1427-1431.
30. Rosas IO, Yao J, Avila NA, Chow CK, Gahl WA, Gochuico BR. Automated quantification of high-resolution CT scan findings in individuals at risk for pulmonary fibrosis. Chest 2011;140:1590-1597.
31. Henske EP, McCormack FX. Lymphangioleiomyomatosis: a wolf in sheep's clothing. J Clin Invest 2012;122:3807-3816.
32. Abbott GF, Rosado-de-Christenson ML, Frazier AA, Franks TJ, Pugatch RD, Galvin JR. From the archives of the AFIP: lymphangioleiomyomatosis: radiologic-pathologic correlation. Radiographics 2005;25:803-828.
33. Cai X, Pacheco-Rodriguez G, Haughey M, Samsel L, Xu S, Wu HP, McCoy JP, Stylianou M, Darling TN, Moss J. Sirolimus decreases circulating lymphangioleiomyomatosis cells in patients with lymphangioleiomyomatosis. Chest 2014;145:108-112.
34. Pacheco-Rodriguez G, Kumaki F, Steagall WK, Zhang Y, Ikeda Y, Lin JP, Billings EM, Moss J. Chemokine-enhanced chemotaxis of lymphangioleiomyomatosis cells with mutations in the tumor suppressor TSC2 gene. J Immunol 2009;182:1270-1277.
35. Chilosi M, Pea M, Martignoni G, Brunelli M, Gobbo S, Poletti V, Bonetti F. Cathepsin-k expression in pulmonary lymphangioleiomyomatosis. Mod Pathol 2009;22:161-166.
36. Hayashi T, Fleming MV, Stetler-Stevenson WG, Liotta LA, Moss J, Ferrans VJ, Travis WD. Immunohistochemical study of matrix metalloproteinases (MMPs) and their tissue inhibitors (TIMPs) in pulmonary lymphangioleiomyomatosis (LAM). Hum Pathol 1997;28:1071-1078.
37. Matsui K, Takeda K, Yu ZX, Travis WD, Moss J, Ferrans VJ. Role for activation of matrix metalloproteinases in the pathogenesis of pulmonary lymphangioleiomyomatosis. Arch Pathol Lab Med 2000;124:267-275.
38. Krymskaya VP, Shipley JM. Lymphangioleiomyomatosis: a complex tale of serum response factor-mediated tissue inhibitor of metalloproteinase-3 regulation. Am J Respir Cell Mol Biol 2003;28:546-550.
39. Zhe X, Yang Y, Jakkaraju S, Schuger L. Tissue inhibitor of metalloproteinase-3 downregulation in lymphangioleiomyomatosis: potential consequence of abnormal serum response factor expression. Am J Respir Cell Mol Biol 2003;28:504-511.
40. Papakonstantinou E, Dionyssopoulos A, Aletras AJ, Pesintzaki C, Minas A, Karakiulakis G. Expression of matrix metalloproteinases and their endogenous tissue inhibitors in skin lesions from patients with tuberous sclerosis. J Am Acad Dermatol 2004;51:526-533.
41. Odajima N, Betsuyaku T, Nasuhara Y, Inoue H, Seyama K, Nishimura M. Matrix metalloproteinases in blood from patients with LAM. Respir Med 2009;103:124-129.
42. Goncharova EA, Goncharov DA, Fehrenbach M, Khavin I, Ducka B, Hino O, Colby TV, Merrilees MJ, Haczku A, Albelda SM, et al. Prevention of alveolar destruction and airspace enlargement in a mouse model of pulmonary lymphangioleiomyomatosis (LAM). Sci Transl Med 2012;4:154ra134.
43. Chang WY, Clements D, Johnson SR. Effect of doxycycline on proliferation, MMP production, and adhesion in LAM-related cells. Am J Physiol Lung Cell Mol Physiol 2010;299:L393-L400.
44. Moir LM, Ng HY, Poniris MH, Santa T, Burgess JK, Oliver BGG, Krymskaya VP, Black JL. Doxycycline inhibits matrix metalloproteinase-2 secretion from TSC2-null mouse embryonic fibroblasts and lymphangioleiomyomatosis cells. Br J Pharmacol 2011;164:83-92.
45. Pimenta SP, Baldi BG, Acencio MM, Kairalla RA, Ribeiro de Carvalho CR. Doxycycline use in patients with lymphangioleiomyomatosis: safety and efficacy in metalloproteinase blockade. J Bras Pneumol 2011;37:424-430.
46. Pimenta SP, Baldi BG, Kairalla RA, Carvalho CR. Doxycycline use in patients with lymphangioleiomyomatosis: biomarkers and pulmonary function response. J Bras Pneumol 2013;39:5-15.
47. Chang WY, Cane JL, Kumaran M, Lewis S, Tattersfield AE, Johnson SR. A 2-year randomised placebo-controlled trial of doxycycline for lymphangioleiomyomatosis. Eur Respir J 2014;43:1114-1123.