293
Views
1
CrossRef citations to date
0
Altmetric
Review

Prospective nanoparticle treatments for lymphangioleiomyomatosis

ORCID Icon, , , ORCID Icon, &
Pages 75-86 | Received 17 Sep 2020, Accepted 11 Jan 2022, Published online: 21 Jan 2022

References

  • Harknett EC, Chang WY, Byrnes S, et al. Use of variability in national and regional data to estimate the prevalence of lymphangioleiomyomatosis. QJM. 2011 Nov;104(11):971–979.
  • Nellist M, Janssen B, Brook-Carter P, et al. Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell. 1993 Dec 31;75(7):1305–1315.
  • Smolarek TA, Wessner LL, McCormack FX, et al. 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 Apr;62(4):810–815.
  • 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 U S A. 2000 May 23;97(11):6085–6090.
  • Goncharova EA, Ammit AJ, Irani C, et al. PI3K is required for proliferation and migration of human pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2002 Aug;283(2):L354–63.
  • Matsui K, Beasley MB, Nelson WK, et al. Prognostic significance of pulmonary lymphangioleiomyomatosis histologic score. Am J Surg Pathol. 2001 Apr;25(4):479–484.
  • Johnson SR, Whale CI, Hubbard RB, et al. Survival and disease progression in UK patients with lymphangioleiomyomatosis. Thorax. 2004 Sep;59(9):800–803.
  • Harari S, Torre O, Cassandro R, et al. The changing face of a rare disease: lymphangioleiomyomatosis. Eur Respir J. 2015;46(5):1471.
  • Moir LM. Lymphangioleiomyomatosis: current understanding and potential treatments. Pharmacol Ther. 2016 Feb;158:114–124.
  • Kumasaka T, Seyama K, Mitani K, et al. Lymphangiogenesis-mediated shedding of LAM cell clusters as a mechanism for dissemination in lymphangioleiomyomatosis. Am J Surg Pathol. 2005 Oct;29(10):1356–1366.
  • Proud CG. mTOR signalling in health and disease. Biochem Soc Trans. 2011 Apr;39(2):431–436.
  • Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol. 2011 Jan;12(1):21–35.
  • Kumasaka T, Seyama K, Mitani K, et al. Lymphangiogenesis in lymphangioleiomyomatosis: its implication in the progression of lymphangioleiomyomatosis. Am J Surg Pathol. 2004 Aug;28(8):1007–1016.
  • Kaipainen A, Korhonen J, Mustonen T, et al. Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3566–3570.
  • Kukk E, Lymboussaki A, Taira S, et al. VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development. 1996 Dec;122(12):3829–3837.
  • Hammer T, Tritsaris K, Hubschmann MV, et al. IL-20 activates human lymphatic endothelial cells causing cell signalling and tube formation. Microvasc Res. 2009 Jun;78(1):25–32.
  • Huber S, Bruns CJ, Schmid G, et al. Inhibition of the mammalian target of rapamycin impedes lymphangiogenesis. Kidney Int. 2007 Apr;71(8):771–777.
  • Ferrans VJ, Yu ZX, Nelson WK, et al. Lymphangioleiomyomatosis (LAM): a review of clinical and morphological features. J Nippon Med Sch. 2000 Oct;67(5):311–329.
  • Johnson SR, Cordier JF, Lazor R, et al. European respiratory society guidelines for the diagnosis and management of lymphangioleiomyomatosis. Eur Respir J. 2010 Jan;35(1):14–26.
  • Cohen MM, Pollock-barziv S, Johnson SR. Emerging clinical picture of lymphangioleiomyomatosis. Thorax. 2005 Oct;60(10):875–879.
  • Stump B, Cui Y, Kidambi P, et al. Lymphatic changes in respiratory diseases: more than just remodeling of the lung? Am J Respir Cell Mol Biol. 2017 Sep;57(3):272–279.
  • Taveira-dasilva AM, Steagall WK, Rabel A, et al. Reversible airflow obstruction in lymphangioleiomyomatosis. Chest. 2009 Dec;136(6):1596–1603.
  • McCormack FX, Inoue Y, Moss J, et al. Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N Engl J Med. 2011 Apr 28;364(17):1595–1606.
  • Kenerson H, Dundon TA, Yeung RS. Effects of rapamycin in the Eker rat model of tuberous sclerosis complex. Pediatr Res. 2005 Jan;57(1):67–75.
  • Bissler JJ, McCormack FX, Young LR, et al. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N Engl J Med. 2008 Jan 10;358(2):140–151.
  • Desai N, Heenan S, Mortimer PS. Sirolimus-associated lymphoedema: eight new cases and a proposed mechanism. Br J Dermatol. 2009 Jun;160(6):1322–1326.
  • Li C, Zhou X, Sun Y, et al. Faslodex inhibits estradiol-induced extracellular matrix dynamics and lung metastasis in a model of lymphangioleiomyomatosis. Am J Respir Cell Mol Biol. 2013;49(1):135–142.
  • Lu C, Lee HS, Pappas GP, et al. A phase II clinical trial of an aromatase inhibitor for postmenopausal women with lymphangioleiomyomatosis. Ann Am Thorac Soc. 2017 Jun;14(6):919–928.
  • Tyryshkin A, Bhattacharya A, Eissa NT. Src kinase is a novel therapeutic target in lymphangioleiomyomatosis. Cancer Res. 2014;74(7):1996.
  • Je DW, YM O, Ji YG, et al. The inhibition of src family kinase suppresses pancreatic cancer cell proliferation, migration, and invasion. Pancreas. 2014;43(5):768–776.
  • Atochina-Vasserman EN, Abramova E, James ML, et al. Pharmacological targeting of VEGFR signaling with axitinib inhibits Tsc2-null lesion growth in the mouse model of lymphangioleiomyomatosis. Am J Physiol Lung Cell Mol Physiol. 2015;309(12):L1447–L54.
  • Atochina-Vasserman EN, Goncharov DA, Volgina AV, et al. Statins in lymphangioleiomyomatosis. Simvastatin and atorvastatin induce differential effects on tuberous sclerosis complex 2-null cell growth and signaling. Am J Respir Cell Mol Biol. 2013 Nov;49(5):704–709.
  • Taveira-dasilva AM, Moss J. Management of lymphangioleiomyomatosis. F1000Prime Rep. 2014;6:116.
  • Finlay GA, Malhowski AJ, Liu Y, et al. Selective inhibition of growth of tuberous sclerosis complex 2 null cells by atorvastatin is associated with impaired rheb and rho GTPase function and reduced mTOR/S6 kinase activity. Cancer Res. 2007;67(20):9878–9886.
  • Goncharova EA, Goncharov DA, Li H, et al. mTORC2 is required for proliferation and survival of TSC2-null cells. Mol Cell Biol. 2011 Jun;31(12):2484–2498.
  • Schraufnagel DE. Lung lymphatic anatomy and correlates. Pathophysiology. 2010 Sep;17(4):337–343.
  • Goncharova EA, Goncharov DA, Fehrenbach M, et al. Prevention of alveolar destruction and airspace enlargement in a mouse model of pulmonary lymphangioleiomyomatosis (LAM). Sci Transl Med. 2012 Oct 3;4(154):154ra34.
  • Pose E, Trebicka J, Mookerjee RP, et al. Statins: old drugs as new therapy for liver diseases? J Hepatol. 2019 Jan;70(1):194–202.
  • Alayev A, Salamon RS, Sun Y, et al. Effects of combining rapamycin and resveratrol on apoptosis and growth of TSC2-deficient xenograft tumors. Am J Respir Cell Mol Biol. 2015 Nov;53(5):637–646.
  • Haeri A, Osouli M, Bayat F, et al. Nanomedicine approaches for sirolimus delivery: a review of pharmaceutical properties and preclinical studies. Artif Cells Nanomed Biotechnol. 2018;46(sup1):1–14.
  • Akbarzadeh A, Rezaei-Sadabady R, Davaran S, et al. Liposome: classification, preparation, and applications. Nanoscale Res Lett. 2013 Feb 22;8(1):102.
  • Daraee H, Etemadi A, Kouhi M, et al. Application of liposomes in medicine and drug delivery. Artif Cells Nanomed Biotechnol. 2016;44(1):381–391.
  • Ghanbarzadeh S, Arami S, Pourmoazzen Z, et al. Improvement of the antiproliferative effect of rapamycin on tumor cell lines by poly (monomethylitaconate)-based pH-sensitive, plasma stable liposomes. Colloids Surf B Biointerfaces. 2014 Mar 1;115:323–330.
  • Haeri A, Sadeghian S, Rabbani S, et al. Use of remote film loading methodology to entrap sirolimus into liposomes: preparation, characterization and in vivo efficacy for treatment of restenosis. Int J Pharm. 2011 Jul 29;414(1–2):16–27.
  • Haeri A, Sadeghian S, Rabbani S, et al. Sirolimus-loaded stealth colloidal systems attenuate neointimal hyperplasia after balloon injury: a comparison of phospholipid micelles and liposomes. Int J Pharm. 2013 Oct 15;455(1–2):320–330.
  • Linares-Alba MA, Gomez-Guajardo MB, Fonzar JF, et al. Preformulation studies of a liposomal formulation containing sirolimus for the treatment of dry eye disease. J Ocul Pharmacol Ther. 2016 Jan-Feb;32(1):11–22.
  • Zhang Y, Huang Y, Li S. Polymeric micelles: nanocarriers for cancer-targeted drug delivery. AAPS PharmSciTech. 2014 Aug;15(4):862–871.
  • Gao X, Huang Y, Makhov AM, et al. Nanoassembly of surfactants with interfacial drug-interactive motifs as tailor-designed drug carriers. Mol Pharm. 2013 Jan 7;10(1):187–198.
  • Zeng S, Xiong MP. Trilayer micelles for combination delivery of rapamycin and siRNA targeting Y-box binding protein-1 (siYB-1). Biomaterials. 2013 Sep;34(28):6882–6892.
  • Acharya S, Dilnawaz F, Sahoo SK. Targeted epidermal growth factor receptor nanoparticle bioconjugates for breast cancer therapy. Biomaterials. 2009 Oct;30(29):5737–5750.
  • Katiyar SS, Muntimadugu E, Rafeeqi TA, et al. Co-delivery of rapamycin- and piperine-loaded polymeric nanoparticles for breast cancer treatment. Drug Deliv. 2016 Sep;23(7):2608–2616.
  • Geszke-Moritz M, Moritz M. Solid lipid nanoparticles as attractive drug vehicles: composition, properties and therapeutic strategies. Mater Sci Eng C Mater Biol Appl. 2016 Nov 1;68:982–994.
  • Singh I, Swami R, Khan W, et al. Lymphatic system: a prospective area for advanced targeting of particulate drug carriers. Expert Opin Drug Deliv. 2014 Feb;11(2):211–229.
  • Mehnert W, Mader K. Solid lipid nanoparticles: production, characterization and applications. Adv Drug Deliv Rev. 2001 Apr 25;47(2–3):165–196.
  • Cai S, Yang Q, Bagby TR, et al. Lymphatic drug delivery using engineered liposomes and solid lipid nanoparticles. Adv Drug Deliv Rev. 2011 Sep 10;63(10–11):901–908.
  • Mishra V, Bansal KK, Verma A, et al. Solid lipid nanoparticles: emerging colloidal nano drug delivery systems. Pharmaceutics. 2018 Oct 18;10(4):191.
  • Manjunath K, Reddy JS, Venkateswarlu V. Solid lipid nanoparticles as drug delivery systems. Methods Find Exp Clin Pharmacol. 2005 Mar;27(2):127–144.
  • Ali Khan A, Mudassir J, Mohtar N, et al. Advanced drug delivery to the lymphatic system: lipid-based nanoformulations. Int J Nanomedicine. 2013;8:2733–2744.
  • Polchi A, Magini A, Mazuryk J, et al. Rapamycin loaded solid lipid nanoparticles as a new tool to deliver mTOR inhibitors: formulation and in vitro characterization. Nanomaterials (Basel). 2016;6(5):87.
  • Mazuryk J, Deptuła T, Polchi A, et al. Rapamycin-loaded solid lipid nanoparticles: morphology and impact of the drug loading on the phase transition between lipid polymorphs. Colloids Surf A Physicochem Eng Asp. 2016 2016/08/05/;502:54–65.
  • Landh E, Moir LM, Gomes Dos Reis L, et al. Inhaled rapamycin solid lipid nano particles for the treatment of Lymphangioleiomyomatosis. Eur J Pharm Sci. 2020 2020/01/15/;142:105098.
  • Landh E, Moir LM, Traini D, et al. Properties of rapamycin solid lipid nanoparticles for lymphatic access through the lungs: part II: the effect of nanoparticle charge. Nanomedicine. 2020;15:1947–1963. ••A two-part research paper that systematically describes the key physical chemical factors that determine the extent of lymphatic update of lipid nanoparticles through the lungs
  • Emoto C, Fukuda T, Cox S, et al. Development of a physiologically-based pharmacokinetic model for sirolimus: predicting bioavailability based on intestinal CYP3A content. CPT Pharmacometrics Syst Pharmacol. 2013;2(7):e59.
  • Freitas CS, Baldi BG, Araújo MS, et al. Use of sirolimus in the treatment of lymphangioleiomyomatosis: favorable responses in patients with different extrapulmonary manifestations. J Bras Pneumol. 2015 May-Jun;41(3):275–280.
  • Taveira-dasilva AM, Hathaway O, Stylianou M, et al. Changes in lung function and chylous effusions in patients with lymphangioleiomyomatosis treated with sirolimus. Ann Intern Med. 2011 Jun 21;154(12:)797–805. w-292-3.
  • Davies DM, de Vries PJ, Johnson SR, et al. Sirolimus therapy for angiomyolipoma in tuberous sclerosis and sporadic lymphangioleiomyomatosis: a phase 2 trial. Clin Cancer Res. 2011 Jun 15;17(12):4071–4081.
  • Ryan GM, Kaminskas LM, Porter CJH. Nano-chemotherapeutics: maximising lymphatic drug exposure to improve the treatment of lymph-metastatic cancers. J Control Release. 2014;193:241–256. 11/10/.
  • Harivardhan Reddy L, Sharma RK, Chuttani K, et al. Influence of administration route on tumor uptake and biodistribution of etoposide loaded solid lipid nanoparticles in dalton’s lymphoma tumor bearing mice. J Control Release. 2005 Jul 20;105(3):185–198.
  • Paliwal R, Rai S, Vaidya B, et al. Effect of lipid core material on characteristics of solid lipid nanoparticles designed for oral lymphatic delivery. Nanomedicine. 2009 Jun;5(2):184–191.
  • Zara GP, Bargoni A, Cavalli R, et al. Pharmacokinetics and tissue distribution of idarubicin-loaded solid lipid nanoparticles after duodenal administration to rats. J Pharm Sci. 2002 May;91(5):1324–1333.
  • Lu B, Xiong SB, Yang H, et al. Solid lipid nanoparticles of mitoxantrone for local injection against breast cancer and its lymph node metastases. Eur J Pharm Sci. 2006 May;28(1–2):86–95.
  • Aji Alex MR, Chacko AJ, Jose S, et al. Lopinavir loaded solid lipid nanoparticles (SLN) for intestinal lymphatic targeting. Eur J Pharm Sci. 2011 Jan 18;42(1–2):11–18.
  • Landh E, Moir LM, Bradbury P, et al. Properties of rapamycin solid lipid nanoparticles for lymphatic access through the lungs: part I: the effect of nanoparticle size. Nanomedicine. 2020;15(20).
  • Hawley AE, Davis SS, Illum L. Targeting of colloids to lymph nodes: influence of lymphatic physiology and colloidal characteristics. Adv Drug Deliv Rev. 1995;17(1):129–148. 1995/10/01/.
  • Junghanns J-UAH, Müller RH. Nanocrystal technology, drug delivery and clinical applications. Int J Nanomedicine. 2008;3(3):295–309.
  • MacDonald A, Scarola J, Burke JT, et al. Clinical pharmacokinetics and therapeutic drug monitoring of sirolimus. Clin Ther. 2000;22(Suppl B):B101–21.
  • Zheng J, Sambol NC, Zimmerman DJ, et al. Population pharmacokinetics (PK) of sirolimus. Clin Pharmacol Ther. 1996;59(2):150
  • Trevaskis NL, Kaminskas LM, Porter CJ. From sewer to saviour - targeting the lymphatic system to promote drug exposure and activity. Nat Rev Drug Discov. 2015 Nov;14(11):781–803.
  • Yáñez JA, Wang SW, Knemeyer IW, et al. Intestinal lymphatic transport for drug delivery. Adv Drug Deliv Rev. 2011 Sep 10;63(10–11):923–942.
  • Trevaskis NL, Charman WN, Porter CJ. Lipid-based delivery systems and intestinal lymphatic drug transport: a mechanistic update. Adv Drug Deliv Rev. 2008 Mar 17;60(6):702–716.
  • Khoo SM, Shackleford DM, Porter CJ, et al. Intestinal lymphatic transport of halofantrine occurs after oral administration of a unit-dose lipid-based formulation to fasted dogs. Pharm Res. 2003 Sep;20(9):1460–1465.
  • Caliph SM, Charman WN, Porter CJH. Effect of short-, medium-, and long-chain fatty acid-based vehicles on the absolute oral bioavailability and intestinal lymphatic transport of halofantrine and assessment of mass balance in lymph-cannulated and non-cannulated rats. J Pharm Sci. 2000;89(8):1073–1084.
  • Anderson M, Omri A. The effect of different lipid components on the in vitro stability and release kinetics of liposome formulations. Drug Deliv. 2004 Jan-Feb;11(1):33–39.
  • Shah R, Eldridge D, Palombo E, et al. Lipid nanoparticles: production, characterization and stability. Switzerland: Springer International Publishing; 2015.
  • Camenisch G, Alsenz J, van de Waterbeemd H, et al. Estimation of permeability by passive diffusion through Caco-2 cell monolayers using the drugs’ lipophilicity and molecular weight. Eur J Pharm Sci. 1998 Oct;6(4):313–319.
  • Singh R, Singh S, Lillard JW Jr. Past, present, and future technologies for oral delivery of therapeutic proteins. J Pharm Sci. 2008 Jul;97(7):2497–2523.
  • Muheem A, Shakeel F, Jahangir MA, et al. A review on the strategies for oral delivery of proteins and peptides and their clinical perspectives. Saudi Pharm J. 2016 Jul;24(4):413–428.
  • Carvalho SR, Watts AB, Peters JI, et al. Characterization and pharmacokinetic analysis of crystalline versus amorphous rapamycin dry powder via pulmonary administration in rats. Eur J Pharm Biopharm. 2014 Sep;88(1):136–147. .
  • Patton JS, Byron PR. Inhaling medicines: delivering drugs to the body through the lungs. Nat Rev Drug Discov. 2007 Jan;6(1):67–74.
  • Landh E, Moir LM, Gomes Dos Reis L, et al. Inhaled rapamycin solid lipid nano particles for the treatment of Lymphangioliomyomatosis. Eur J Pharm Sci. 2019;142:105098.
  • Videira MA, Botelho MF, Santos AC, et al. Lymphatic uptake of pulmonary delivered radiolabelled solid lipid nanoparticles. J Drug Target. 2002 Dec;10(8):607–613.
  • Rabaça Roque Botelho MF, Tavares Marques MA, Freitas Gomes CM, et al. Nanoradioliposomes molecularly modulated to study the lung deep lymphatic drainage. Rev Port Pneumol. 2009 Mar-Apr;15(2):261–293.
  • Mohammad AK, Amayreh LK, Mazzara JM, et al. Rapid lymph accumulation of polystyrene nanoparticles following pulmonary administration. Pharm Res. 2013 Feb;30(2):424–434.
  • Lipp MM, Kamerkar A. inventors; Rapamycin powders for pulmonary delivery. United States; 2016.
  • Raimondi A, Colombo F, Pintarelli G, et al. Prolonged activity and toxicity of sirolimus in a patient with metastatic renal perivascular epithelioid cell tumor: a case report and literature review. Anticancer Drugs. 2018 Jul;29(6):589–595.
  • Yao J, Taveira-dasilva AM, Jones AM, et al. Sustained effects of sirolimus on lung function and cystic lung lesions in lymphangioleiomyomatosis. Am J Respir Crit Care Med. 2014 Dec 1;190(11):1273–1282.
  • Khalili Fard J, Jafari S, Eghbal MA. A review of molecular mechanisms involved in toxicity of nanoparticles. Adv Pharm Bull. 2015 Nov;5(4):447–454.
  • Matuszak J, Baumgartner J, Zaloga J, et al. Nanoparticles for intravascular applications: physicochemical characterization and cytotoxicity testing. Nanomedicine (Lond). 2016 Mar;11(6):597–616.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.