Clathrin-independent endocytosis – role in disease processes and pharmaceutical aspects

COMMENTARY ON THE LAW

Clathrin-independent endocytosis – role in disease processes and pharmaceutical aspects

Bogusława Konopska 1 , Krzysztof Gołąb 1 , Jakub Gburek 1

1. Katedra i Zakład Biochemii Farmaceutycznej, Uniwersytet Medyczny im. Piastów Śląskich we Wrocławiu

Published: 2015-07-07
DOI: 10.5604/17322693.1160614
GICID: 01.3001.0009.6549
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2015; 69 : 763-776

 

Abstract

Clathrin-independent endocytosis (CIE) is the process of cellular uptake of various particles, including pathogens, without the coat protein clathrin. It occurs commonly in mammalian cells and is regulated by protein-lipid composition of the cell membranes. Understanding of different routes of CIE allowed the identification of novel molecular mechanisms involved in uptake of molecules and cell signaling and explained their role in pathological processes. In this paper we characterize diseases associated with genetic defects of proteins involved in CIE and the relationship between expression of these proteins and pathology of atherosclerosis, hypercholesterolemia, diabetes and neoplasia. The role of CIE in bacterial, viral, fungal, and protozoal infections is also presented. In the second part we describe the plausible use of clathrin-independent endocytosis in increasing drug absorption, their penetration through biological membranes, and the design of specific nanocarriers for selective cell uptake.

References

  • 1. Aït-Slimane T., Galmes R., Trugnan G., Maurice M.: Basolateralinternalization of GPI-anchored proteins occurs via a clathrin-independentflotillin-dependent pathway in polarized hepatic cells.Mol. Biol. Cell., 2009; 20: 3792-3800
    Google Scholar
  • 2. Ba Q., Zhou N., Duan J., Chen T., Hao M., Yang X., Li J., Yin J., ChuR., Wang H.: Dihydroartemisinin exerts its anticancer activity troughdepleting cellular iron via transferrin receptor-1. PLoS One,2012; 7: e42703
    Google Scholar
  • 3. Briand N., Dugail I., Le Lay S.: Cavin proteins: new players in thecaveolae field. Biochimie, 2011; 93: 71-77
    Google Scholar
  • 4. Canton I., Battaglia G.: Endocytosis at the nanoscale. Chem. Soc.Rev., 2012; 41: 2718-2739
    Google Scholar
  • 5. Chang S.H., Feng D., Nagy J.A., Sciuto T.E., Dvorak A.M., DvorakH.F.: Vascular permeability and pathological angiogenesis in caveolin-1-nullmice. Am. J. Pathol., 2009; 175: 1768-1776
    Google Scholar
  • 6. Chaudhary N., Gomez G.A., Howes M.T., Lo H.P., McMahon K.A.,Rae J.A., Schieber N.L., Hill M.M., Gaus C., Yap A.S., Parton R.G.: Endocyticcrosstalk: cavins, caveolins, and caveolae regulate clathrin–independent endocytosis. PLoS Biol., 2014; 12: e1001832
    Google Scholar
  • 7. Chi P.I., Liu H.J.: Molecular signaling and cellular pathways forvirus entry. ISRN Virology, 2013, 2013; ID 306595
    Google Scholar
  • 8. Collins R.F., Touret N., Kuwata H., Tandon N.N., Grinstein S., TrimbleW.S.: Uptake of oxidized low density lipoprotein by CD36 occursby an actin-dependent pathway distinct from macropinocytosis. J.Biol. Chem., 2009; 284: 30288-30297
    Google Scholar
  • 9. Coppens I., Sinai A.P., Joiner K.A.: Toxoplasma gondii exploitshost low density lipoprotein receptor-mediated endocytosis forcholesterol acquisition. J. Cell Biol., 2000; 149: 167-180
    Google Scholar
  • 10. Damm E-M., Pelkmans L., Kartenbeck J., Mezzacasa A., KurzchaliaT., Helenius A.: Clathrin- and caveolin-1-independent endocytosis:entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol.,2005; 168: 477-488
    Google Scholar
  • 11. de Vries E., Tscherne D.M., Wienholts M.J., Cobos-Jiménez V.,Scholte F., García-Sastre A., Rottier P.J., de Haan C.A.: Dissection ofthe influenza A virus endocytic routes reveals macropinocytosisas an alternative entry pathway. PLoS Pathog., 2011; 7: e1001329
    Google Scholar
  • 12. Delmas D., Aires V., Colin D.J., Limagne E., Scagliarini A., CotteA.K., Ghiringhelli F.: Importance of lipid microdomains, rafts, inabsorption, delivery, and biological effects of resveratrol. Ann. N.Y.Acad. Sci., 2013; 1290: 90-97
    Google Scholar
  • 13. DeWever J., Frerart F., Bouzin C., Baudelet C., Ansiaux R., SonveauxP., Gallez B., Dessy C., Feron O.: Caveolin-1 is critical for the maturationof tumour blood vessels through the regulation of both endothelial tubeformation and mural cell recruitment. Am. J. Pathol., 2007; 171: 1619-1628
    Google Scholar
  • 14. Doherty G.J., McMahon H.T.: Mechanisms of endocytosis. Annu.Rev. Biochem., 2009; 78: 857-902
    Google Scholar
  • 15. Duncan R., Richardson S.C.: Endocytosis and intracellular traffickingas gateways for nanomedicine delivery: opportunities andchallenges. Mol. Pharm., 2012; 9: 2380-2402 16 Eierhoff T., Stechmann B., Rӧmer W.: Pathogen and toxin entry- how pathogens and toxins induce and harness endocytoticmechanisms. W: Molecular regulation of endocytosis, Wyd. BrianCeresa, 2012, 251-276
    Google Scholar
  • 16. by actin-dependent, clathrin- and lipid raft-independent endocytosis.PLoS Pathog., 2012; 8: e1002657
    Google Scholar
  • 17. Elsadek B., Kratz F.: Impact of albumin of drug delivery – Newapplications on the horizon. J. Control. Release, 2012; 157: 4-28
    Google Scholar
  • 18. Ewers H., Römer W., Smith A.E., Bacia K., Dmitrieff S., Chai W.,Mancini R., Kartenbeck J., Chambon V., Berland L., Oppenheim A.,Schwarzmann G., Feizi T., Schwille P., Sens P., Helenius A., JohannesL.: GM1 structure determines SV40-induced membrane invaginationand infection. Nat. Cell Biol., 2010; 12: 11-18; sup 1-12
    Google Scholar
  • 19. Gadjeva M., Paradis-Bleau C., Priebe G.P., Fichorova R., Pier G.B.:Caveolin-1 modifies the immunity to Pseudomonas aeruginosa. J.Immunol., 2010; 184: 296-302
    Google Scholar
  • 20. Galbiati F., Volonte D., Chu J.B., Li M., Fine S.W., Fu M., BermudezJ., Pedemonte M., Weidenheim K.M., Pestell R.G., Minetti C., LisantiM.P.: Transgenic overexpression of caveolin-3 in skeletal muscle fibresinduces a Duchenne-like muscular dystrophy phenotype. Proc.Natl. Acad. Sci. USA, 2000; 97: 9689-9694
    Google Scholar
  • 21. Gallicchio M.A., Bach L.A.: Uptake of advanced glycation endproducts by proximal tubule epithelial cells via macropinocytosis.Biochim. Biophys. Acta, 2013; 1833: 2922-2932
    Google Scholar
  • 22. Ham H., Sreelatha A., Orth K.: Manipulation of host membranesby bacterial effectors. Nat. Rev. Microbiol., 2011; 9: 635-646
    Google Scholar
  • 23. Horonchik L., Wessling-Resnick M.: The small-molecule irontransport inhibitor ferristatin/NSC306711 promotes degradation ofthe transferrin receptor. Chem. Biol., 2008; 15: 647-653
    Google Scholar
  • 24. Howes M.T., Mayor S., Parton R.G.: Molecules, mechanisms, andcellular roles of clathrin-independent endocytosis. Curr. Opin. CellBiol., 2010; 22: 519-527
    Google Scholar
  • 25. Hsu J., Rappaport J., Muro S.: Specific binding, uptake, and transportof ICAM-1-targeted nanocarriers across endothelial and subendothelialcell components of the blood-brain barrier. Pharm. Res.,2014; 31: 1855-1866
    Google Scholar
  • 26. Jones A.R, Shusta E.V.: Blood-brain barrier transport of therapeuticsvia receptor mediation. Pharm. Res., 2007; 24: 1759-1771
    Google Scholar
  • 27. Kastl L., Sasse D., Wulf V., Hartmann R., Mircheski J., Ranke C.,Carregal-Romero S., Martínez-López J.A., Fernández-Chacón R., ParakW.J., Elsasser H.P., Rivera Gil P.: Multiple internalization pathwaysof polyelectrolyte multilayer capsules into mammalian cells.ACS Nano, 2013; 7: 6605-6618
    Google Scholar
  • 28. Konopska B., Gołąb K., Gburek J.: Endocytoza niezależna od klatryny– co wiemy, co przypuszczamy, co pozostaje zagadką. PostępyBiol. Kom., 2014; 41: 265-284
    Google Scholar
  • 29. Korhonen J.T., Puolakkainen M., Häivälä R., Penttilä T., HaveriA., Markkula E., Lahesmaa R.: Flotillin-1 (Reggie-2) contributes toChlamydia pneumoniae growth and is associated with bacterial inclusion.Infect. Immun., 2012; 80: 1072-1078
    Google Scholar
  • 30. Korhonen J.T., Puolakkainen M., Haveri A., Tammiruusu A., SarvasM., Lahesmaa R.: Chlamydia pneumoniae entry into epithelial cells byclathrin-independent endocytosis. Microb. Pathog., 2012; 52: 157-164
    Google Scholar
  • 31. Kuliczkowska-Płaksej J., Bednarek-Tupikowska G., Płaksej R.,Filus A.: Receptor CD36 – występowanie, regulacja ekspresji orazrola w patogenezie miażdżycy. Część I. Postępy Hig. Med. Dośw.,2006; 60: 142-151
    Google Scholar
  • 32. Kumari S., Mg S., Mayor S.: Endocytosis unplugged: multipleways to enter the cell. Cell Res., 2010; 20: 256-275
    Google Scholar
  • 33. Laurenzana A., Fibbi G., Chilla A., Margheri G., Del Rosso T., RovidaE., Del Rosso M., Margheri F.: Lipid rafts: integrated platformsfor vascular organization offering therapeutic opportunities. Cell.Mol. Life Sci., 2015; 72: 1537-1557
    Google Scholar
  • 34. Lin, M.I., Yu J., Murata T., Sessa W.C.: Caveolin-1-deficient micehave increased tumor microvascular permeability, angiogenesis, andgrowth. Cancer Res., 2007; 67: 2849-2856
    Google Scholar
  • 35. Machado F.S., Rodriguez N.E., Adesse D., Garzoni L.R., Esper L.,Lisanti M.P., Burk R.D., Albanese C., Van Doorslaer K., Weiss L.M.,Nagajyoyhi F., Nosanchuk J.D., Wilson M.E., Tanowitz H.B.: Recentdevelopments in the interactions between caveolin and pathogens.Adv. Exp. Med. Biol., 2012; 729: 65-82
    Google Scholar
  • 36. Maldonado-Báez L., Williamson C., Donaldson J.G.: Clathrin-independentendocytosis: a cargo-centric view. Exp. Cell Res., 2013;319: 2759-2769
    Google Scholar
  • 37. Malik A.B.: Targeting endothelial cell surface receptors: novelmechanisms of microvascular endothelial barrier transport. J. Med.Sci., 2009; 2: 13-17
    Google Scholar
  • 38. Matsuda M., Suzuki R., Kataoka C, Watashi K., Aizaki H., KatoN., Matsuura Y., Suzuki T., Wakita T.: Alternative endocytosis pathwayfor productive entry of hepatitis C virus. J. Gen. Virol., 2014;95: 2658-2667
    Google Scholar
  • 39. Maza P.K., Straus A.H., Toledo M.S., Takahashi H.K., Suzuki E.:Interaction of epithelial cell membrane rafts with Paracoccidioidesbrasiliensis leads to fungal adhesion and Src-family kinase activation.Microbes Infect., 2008; 10: 540-547
    Google Scholar
  • 40. Mercer J., Helenius A.: Virus entry by macropinocytosis. Nat.Cell Biol., 2009; 11: 510-520
    Google Scholar
  • 41. Michel V., Bakovic M.: Lipid rafts in health and disease. Biol.Cell, 2007; 99: 129-140
    Google Scholar
  • 42. Mosesson Y., Mills G.B., Yarden Y.: Derailed endocytosis: an emergingfeature of cancer. Nat. Rev. Cancer, 2008; 8: 835-850
    Google Scholar
  • 43. Muro S., Wiewrodt R., Thomas A., Koniaris L., Albelda S.M., MuzykantovV.R., Koval M.: A novel endocytic pathway induced by clusteringendothelial ICAM-1 or PECAM-1. J. Cell Sci., 2003; 116: 1599-1609
    Google Scholar
  • 44. Orth J.D., McNiven M.A.: Get off my back! Rapid receptor internalizationthrough circular dorsal ruffles. Cancer Res., 2006; 66:11094-11096
    Google Scholar
  • 45. Otto G.P., Nichols B.J.: The roles of flotillin microdomains – endocytosisand beyond. J. Cell Sci., 2011; 124: 3933-3940
    Google Scholar
  • 46. Parton R.G., del Pozo M.A.: Caveolae as plasma membrane sensors,protectors and organizers. Nat. Rev. Mol. Cell Biol., 2013; 14:98-112
    Google Scholar
  • 47. Patel H.H., Murray F., Insel P.A.: Caveolae as organizers of pharmacologicallyrelevant signal transduction molecules. Annu. Rev.Pharmacol. Toxicol., 2008; 48: 359-391
    Google Scholar
  • 48. Payne C.K, Jones S.A., Chen C., Zhuang X.: Internalization andtrafficking of cell surface proteoglycans and proteoglycan-bindingligands. Traffic, 2007; 8: 389-401
    Google Scholar
  • 49. Plummer E.M., Manchester M.: Endocytic uptake pathways utilizedby CPMV nanoparticles. Mol. Pharm., 2013; 10: 26-32
    Google Scholar
  • 50. Premont R.T., Schmalzigaug R.: Metastasis: wherefore arf thou?Curr. Biol., 2009; 19: R1036-R1038
    Google Scholar
  • 51. Radin N.S.: Preventing the binding of pathogens to the hostby controlling sphingolipid metabolism. Microbes Infect., 2006; 8:938-945
    Google Scholar
  • 52. Rahman A., Sward K.: The role of caveolin-1 in cardiovascularregulation. Acta Physiol., 2009; 195: 231-245
    Google Scholar
  • 53. Rajab A., Straub V., McCann L.J., Seelow D., Varon R., Barresi R.,Schulze A., Lucke B., Lutzkendorf S., Karbasiyan M., Bachmann S.,Spuler S., Schuelke M.: Fatal cardiac arrhythmia and long-QT syndromein a new form of congenital generalized lipodystrophy withmuscle rippling (CGL4) due to PTRF-CAVIN mutations. PLoS Genet.,2010; 6: e1000874
    Google Scholar
  • 54. Rajendran L., Knölker H.J., Simons K.: Subcellular targeting strategiesfor drug design and delivery. Nat. Rev. Drug Discov., 2010; 9: 29-42
    Google Scholar
  • 55. Rajendran L., Udayar V., Goodger Z.V.: Lipid-anchored drugs fordelivery into subcellular compartments. Trends Pharmacol. Sci.,2012; 33: 215-222
    Google Scholar
  • 56. Roth D.M., Patel H.H.: Role of caveolae in cardiac protection.Pediatr. Cardiol., 2011; 32: 329-333
    Google Scholar
  • 57. Sahay G., Alakhova D., Kabanov A.V.: Endocytosis of nanomedicines.J. Control. Release, 2010; 145: 182-195
    Google Scholar
  • 58. Schelhaas M., Shah B., Holzer M., Blattmann P., Kühling L., DayP.M., Schiller J.T., Helenius A.: Entry of human papillomavirus type
    Google Scholar
  • 59. Schmees C., Villasenor R., Zheng W., Ma H., Zerial M., HeldinC.H., Hellberg C.: Macropinocytosis of the PDGF β-receptor promotesfibroblast transformation by H-RasG12V. Mol. Biol. Cell, 2012;23: 2571-2582
    Google Scholar
  • 60. Schweitzer J.K., Sedgwick A.E., D’Souza-Schorey C:. ARF6-mediatedendocytic recycling impacts cell movement, cell division andlipid homeostasis. Semin. Cell Dev. Biol., 2011; 22: 39-47
    Google Scholar
  • 61. Schwencke C., Braun-Dullaeus R.C., Wunderlich C., Strasser R.H.:Caveolae and caveolin in transmembrane signaling – implicationsfor human disease. Cardiovasc. Res., 2006; 70: 42-49
    Google Scholar
  • 62. Scotti E., Calamai M., Goulbourne C.N., Zhang L., Hong C., LinR.R., Choi J., Pilch P.F., Fong L.G., Zou P., Ting A.Y., Pavone F.S., YoungS.G., Tontonoz P.: IDOL stimulates clathrin-independent endocytosisand multivesicular body-mediated lysosomal degradation of thelow-density lipoprotein receptor. Mol. Cell. Biol., 2013; 33: 1503-1514
    Google Scholar
  • 63. Sellers S.L., Trane A.E., Bernatchez P.N.: Caveolin as a potentialdrug target for cardiovascular protection. Front. Physiol., 2012; 3: 280
    Google Scholar
  • 64. Simons K., Sampaio J.L.: Membrane organization and lipid rafts.Cold Spring Harb. Perspect. Biol., 2011; 3: a004697
    Google Scholar
  • 65. Sotgia F., Martinez-Outschoorn U.E., Howell A., Pestell R.G., PavlidesS., Lisanti M.P.: Caveolin-1 and cancer metabolism in the tumormicroenvironment: markers, models, and mechanisms. Annu.Rev. Pathol., 2012; 7: 423-467
    Google Scholar
  • 66. Sowa G.: Caveolae, caveolins, cavins, and endothelial cell function:new insights. Front. Physiol., 2012; 2: 120
    Google Scholar
  • 67. Srikanth C.V., Mercado-Lubo R., Hallstrom K., McCormick B.A.:Salmonella effector proteins and host-cell responses. Cell. Mol. LifeSci., 2011, 68: 3687-3697
    Google Scholar
  • 68. Tagawa M., Ueyama T., Ogata T., Takehara N., Nakajima N., IsodonoK., Asada S., Takahashi T., Matsubara H., Oh H.: MURC, a muscle-restrictedcoiled-coil protein, is involved in the regulation of skeletalmyogenesis. Am. J. Physiol. Cell Physiol., 2008; 295: C490-C498
    Google Scholar
  • 69. Tiruppathi C., Song W., Bergenfeldt M., Sass P., Malik A.B.: Gp60activation mediates albumin transcytosis in endothelial cells by tyrosinekinase-dependent pathway. J. Biol. Chem., 1997; 272: 25968-25975
    Google Scholar
  • 70. Tsutsumi Y.M., Horikawa Y.T., Jennings M.M., Kidd M.W., NiesmanI.R., Yokoyama U., Head B.P., Hagiwara Y., Ishikawa Y., Miyanohara A., Patel P.M., Insel P.A., Patel H.H., Roth D.M.: Cardiac–specific overexpression of caveolin-3 induces endogenous cardiacprotection by mimicking ischemic preconditioning. Circulation,2008; 118: 1979-1988
    Google Scholar
  • 71. Williams J.J., Palmer T.M.: Cavin-1: caveolae-dependent signallingand cardiovascular disease. Biochem. Soc. Trans., 2014; 42: 284-288
    Google Scholar
  • 72. Wojewódzka U., Gajkowska B., Jurkiewicz J., Gniadecki R.: Mikrodomeny(rafty) lipidowe w błonach komórkowych: struktura,fizjologia i znaczenie w procesach patologicznych. Postępy Biol.Kom., 2005, 32, 293-309
    Google Scholar
  • 73. Xia F., Li R., Wang C., Yang S., Tian L., Dong H., Pei C., He S., JiangP., Cheng H., Fang S., Li H., Xu H.: IRGM1 regulates oxidized LDLuptake by macrophage via actin-dependent receptor internalizationduring atherosclerosis. Sci. Rep., 2013; 3: 1867
    Google Scholar
  • 74. Yang H.L., Chen W.Q., Cao X., Worschech A., Du L.F., Fang W.Y.,Xu Y.Y., Stroncek D.F., Li X., Wang E., Marincola F.M.: Caveolin-1 enhancesresveratrol-mediated cytotoxicity and transport in a hepatocellularcarcinoma model. J. Transl. Med., 2009; 7: 22
    Google Scholar
  • 75. Yoon D.J., Liu C.T., Quinlan D.S., Nafisi P.M., Kamei D.T.: Intracellulartrafficking considerations in the development of naturalligand-drug molecular conjugates for cancer. Ann. Biomed. Eng.,2011; 39: 1235-1251
    Google Scholar
  • 76. Zhou J.X., Liao D., Zhang S., Cheng N., He H.Q., Ye R.D.: ChemerinC9 peptide induces receptor internalization through a clathrin-independentpathway. Acta Pharmacol. Sin., 2014; 35: 653-663
    Google Scholar

Full text

Skip to content