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(12) United States Patent (10) Patent No.: US 8,999,716 B2 Gundlach Et Al

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(12) United States Patent (10) Patent No.: US 8,999,716 B2 Gundlach Et Al US0089997 16B2 (12) United States Patent (10) Patent No.: US 8,999,716 B2 Gundlach et al. (45) Date of Patent: Apr. 7, 2015 (54) ARTIFICIAL MYCOLIC ACID MEMBRANES USPC ..................................... 977/712 714; 436/71 See application file for complete search history. (75) Inventors: Jens Gundlach, Seattle, WA (US); Ian M. Derrington, Seattle, WA (US); Kyle W. Langford, University Place, WA (56) References Cited (US) U.S. PATENT DOCUMENTS (73) Assignee: University of Washington, Seattle, WA 6,171,830 B1* 1/2001 Verschoor ..................... 435.134 (US) 6,406,880 B1 6/2002 Thornton 2002/0052412 A1* 5/2002 Verschoor et al. ............ 514/557 - r 2004, OO63200 A1 4/2004 Chaikof (*) Notice: sity is titly 2006/0008519 A1 1/2006 Davidsen et al. ............. 424/450 U.S.C. 154(b) by 0 days. (Continued) (21) Appl. No.: 13/592,030 FOREIGN PATENT DOCUMENTS JP O7-248329 A 9, 1995 (22) Filed: Aug. 22, 2012 WO 2007041621 A2 4, 2007 (65) Prior Publication Data OTHER PUBLICATIONS US 2013/0146456A1 Jun. 13, 2013 Butler, T. Z. et al. “Single-molecule DNA detection with an engi Related U.S. Application Data neered MspA protein nanopore'. Proceedings of the National Acad .S. App emy of Science USA, vol. 105, No. 52, Dec. 30, 2008, p. 20647 (63) Continuation of application No. 2O652* PCT/US2011/025960, filed on Feb. 23, 2011. (Continued) (60) Provisional application No. 61/307,441, filed on Feb. fEEE application No. 61/375,707, Primary Examiner — J. Christopher Ball • 1- ws (74) Attorney, Agent, or Firm — Christensen O'Connor (51) Int. Cl. Johnson Kindness PLLC GOIN 27/2447 (2006.01) GOIN 33/487 (2006.01) (57) ABSTRACT B82Y5/00 (2011.01) (52) U.S. Cl. Provided herein are artificial membranes of mycolic acids. CPC G0IN 27/447 (2013.01); G0IN 33/48721 The membranes may be unsupported or tethered. These mem - - - - - (2013,01). GOIN 2 74.1704 (2013.01); B82Y branes are long lived and highly resistant to electroporation, 5/00 (2013 61); Y10S 977/781 (2013 013: YIOS demonstrating their general strength. The mycolic acid mem 977/924 (2013 .01); Y10S 977/712 (20 13 .01): branes are suitable for controlled studies of the mycobacterial s Y10S 977/714 (2013 01) outer membrane and can be used in other experiments, such (58) Field of Classification Search as nanopore analyte translocation experiments. CPC ................. C11C 1/00-1/06; C11C3/003/14: CO7D 3O3/38 303/48 19 Claims, 6 Drawing Sheets MADPhPCRUPTURECOMPARISON DPhPCBREAKOWN DMABREAKDOWN al 2.5 3 3.5 4 VIVOLTS) US 8,999,716 B2 Page 2 (56) References Cited International Preliminary Report on Patentability mailed Aug. 28. 2012, issued in International Application No. PCT/US2011/025963, U.S. PATENT DOCUMENTS filed Feb. 23, 2011, 6 pages. Notification of the First Office Action mailed Oct. 8, 2013, issued in 2007/O190542 A1 8/2007 Ling 2007,0269843 A1 11/2007 Thornton the Chinese Application No. 201180018449.5, filed Feb. 23, 2011, 6 2009,0298072 A1 12, 2009 Ju pageS. 2011/O150981 A1* 6, 2011 Baird et al. ................... 424/450 Notification of the First Office Action mailed Apr. 23, 2014, issued in OTHER PUBLICATIONS corresponding Chinese Application No. 201180018451.2, filed Feb. 23, 2011, 7 pages. International Search Report and Written Opinion mailed Dec. 7. Notification of the Third Office Action mailed Oct. 29, 2014, issued 2011, issued in corresponding International Application No. PCT/ in Chinese Patent Application No. 201180018449.5, filed Feb. 23, US2011/025960, filed Feb. 23, 2011, 6 pages. 2011, 3 pages. Rhee, M., and M.A. Burns, “Nanopore Sequencing Technology: Research Trends and Applications. Trends in Biotechnology Notification of the Second Office Action mailed Dec. 3, 2014, issued 24(12):580-586, Dec. 2006. in corresponding Chinese Patent Application No. 201180018451.2, International Search Report and Written Opinion mailed Nov. 28. filed Feb. 23, 2011, 10 pages. 2011, issued in International Application No. PCT/US2011/025963, filed Feb. 23, 2011, 9 pages. * cited by examiner U.S. Patent Apr. 7, 2015 Sheet 1 of 6 US 8,999,716 B2 O O O O HO OH HO OH HO OH HO OH O MeO Keto Alpha Methoxy U.S. Patent Apr. 7, 2015 Sheet 2 of 6 US 8,999,716 B2 STEPWISE INSERTIONS OF MspAINTO MAMEMBRANES 11 O2 8 46 O 4 8 12 16 TIME (s) U.S. Patent Apr. 7, 2015 Sheet 3 of 6 US 8,999,716 B2 MA 8 DPhPCRUPTURE COMPARISON MABREAKDOWN INTOOCIETV/OS Si|lo 2 2.5 3 3.5 4 VIVOLTS) U.S. Patent Apr. 7, 2015 Sheet 4 of 6 US 8,999,716 B2 MspA IV CURVE INDPPC AND MABILAYERS 400 300 2 O O 100 O 50 100 150 200 VOLTS (mV) U.S. Patent Apr. 7, 2015 Sheet 5 of 6 US 8,999,716 B2 MspA MEMBRANE U.S. Patent Apr. 7, 2015 Sheet 6 of 6 US 8,999,716 B2 POLYAHAIRPIN BLOCKAGE DEPTH 4 O MspAINDPhPC O MspAINMYCOLIC ACID O O 5 2 0. 5 100 150 200 250 300 350 400 450 VOLTAGE (mV) 2.6 US 8,999,716 B2 1. 2 ARTIFICIAL MYCOLIC ACID MEMBRANES Other embodiments provide an artificial membrane consist ing essentially of a plurality of mycolic acids and a nanopore. CROSS-REFERENCES TO RELATED Other embodiments provide an artificial membrane consist APPLICATIONS ing essentially of a plurality of mycolic acids, admixtures of other lipids, and a nanopore. This application is a continuation of International Appli Further provided is a system comprising an artificial mem cation No. PCT/US2011/025960, filed Feb. 23, 2011, which brane comprising a mycolic acid positioned between a first claims the benefit of U.S. Provisional Application Ser. No. liquid conductive medium and a second liquid conductive 61/307,441, filed Feb. 23, 2010, and U.S. Provisional Appli medium. Also provided are methods comprising applying an cation Ser. No. 61/375,707, filed Aug. 20, 2010, each of electric field to the system. which is incorporated herein by reference in its entirety. Methods of preparing artificial unsupported mycolic mem branes comprising a mycolic acid are also provided. One STATEMENT OF GOVERNMENT LICENSE embodiment provides a method of making an artificial unsup RIGHTS ported membrane comprising a mycolic acid, comprising: (a) 15 pretreating an aperture of about 500 nm to about 500 um in This invention was made with Government support under diameter with one or more coats of a mycolic acids-hexane Grant Numbers R01 HGOO5115 and 5R21 HGOO4145 mixture and removing the hexane to provide dry mycolic awarded by the National Institutes of Health. The Govern acids; (b) applying a hydrocarbon Solvent to the dry mycolic ment has certain rights in the invention. acids followed by heating to promote hydrocarbon solvent incorporation to provide a mycolic acids-hydrocarbon Sol BACKGROUND vent composition; (c) placing the aperture between a first liquid conductive medium and a second liquid conductive Mycobacteria, including Mycobacterium tuberculosis, medium; (d) applying the mycolic acids-hydrocarbon Solvent have developed strains that resist contemporary multi-drug composition to the aperture while monitoring an ion current treatment regimes. With nearly two million yearly deaths 25 through the aperture until aperture resistance increases to caused by infections of M. tuberculosis and with more than above 1 TC2, followed by forcing one of the liquid conductive 200,000 people debilitated by infections of M. lepraethere is mediums through the aperture from the trans side to eliminate concerted need to understand the mechanisms of Mycobac ion current blockage as needed; and (e) placing an air bubble terial resilience. Part of the persistence and lethality of these over the aperture followed by retraction of the air bubble, diseases is due to the impermeable mycobacteria cell wall. 30 wherein membrane formation is indicated by the aperture Mycobacteria's unique -8 nm thick outer cellular casing has resistance increasing to above 1 TC2, and wherein bilayer far lower permeability to hydrophilic agents than Escherichia membrane formation is indicated if a nanopore can form coli's cell wall and is a key factor in the drug and environ within the membrane. mental resistance of mycobacteria. Although containing other constituents, the mycobacterial 35 DESCRIPTION OF THE DRAWINGS outer membrane contains 30%-40% mycolic acids. Mycolic acids contain a carboxylic acid headgroup with two hydro The foregoing aspects and many of the attendant advan phobic tails of unequal length. See FIG. 1 for exemplary tages of this invention will become more readily appreciated mycolic acids. In vivo, mycolic acids are covalently linked by as the same become better understood by reference to the the carboxylate group to peptidoglycans or trehalose Sugars. 40 following detailed description, when taken in conjunction The significant impermeability of the mycobacterial mem with the accompanying drawings. branes results in the need for pathways for hydrophilic sol FIG. 1 shows the chemical structures of exemplary mycolic utes. This pathway is mediated by protein pores. acids present in mycobacterial outer membranes. See Annu In vivo studies of pore proteins in the mycobacterial cell Rev Biochem 64:29 (1995). wall of M. Smegmatis, a close relative of M. tuberculosis, led 45 FIG. 2 shows change in conductivity across mycolic acid to the discovery of the outer membrane pore M. Smegmatis (MA) membranes with discrete current steps after the addi porin A (MspA). In M. Smegmatis, MspA is the most abun tion of MspA. The observed current steps are indistinguish dant protein and forms the primary pathway for hydrophilic able from current levels observed in DPhPC membranes. nutrients to traverse the outer membrane. OmpATb, another FIG.3 shows the scaled histograms of rupture voltages of protein pore, and ion transporters have been isolated in myco 50 MA membranes (N=330) and DPhPC membranes (N=205) bacterium species but their behavior in their natural environ and includes data from several different ~20 um apertures.
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