Molecular Interactions During Borrelia burgdorferi Migration from the Vector to the Mammalian Nervous System

Manzama-Esso      Abi; Zhenhua       Ji; Miaomiao       Jian; Xiting       Dai; Ruolan       Bai; Zhe       Ding; Lisha        Luo; Taigui       Chen; Feng       Wang; Shiyuan       Wen; Guozhong       Zhou; Fukai       Bao; Aihua       Liu
doi:10.2174/1389203720666191015145714
Abstract

Lyme disease (LD) is an infectious disease caused by the spirochetes of genus borrelia, which are transmitted by the ticks of the genus ixodes. LD is transmitted by the spirochete B. burgdorferi sensu lato. Once in contact with the host through a tick bite, the pathogen comes into contact with the host defense, and must escape this machinery to establish LD, thus using a large number of mechanisms involving the vector of the pathogen, the pathogen itself and also the host. The initial diagnosis of the disease can be made based on the clinical symptoms of LD and the disease can be treated and cured with antibiotics if the diagnosis is made early in the beginning of the disease. Contrariwise, if LD is left untreated, the pathogen disseminates throughout the tissues and organs of the body, where it establishes different types of disease manifestations. In the nervous system, the inflammation caused by B. burgdorferi is known as Lyme neuroborreliosis (LNB). LNB is one of the principal manifestations of LD. In this review, we systematically describe the different molecular interactions among B. burgdorferi, the vector (tick) and the mammalian host.
Keywords: Lyme borreliosis, Lyme neuroborreliosis, tick, B. burgdorferi, mammal host, molecular interaction.
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Graphical Abstract

[1] 
Steere, A.C.; Malawista, S.E.; Snydman, D.R.; Shope, R.E.; Andiman, W.A.; Ross, M.R.; Steele, F.M. Lyme arthritis: an epidemic of oligoarticular arthritis in children and adults in three connecticut communities. Arthritis Rheum.,  1977, 20(1), 7-17.
[http://dx.doi.org/10.1002/art.1780200102] [PMID: 836338] 
[2] 
Steere, A.C. Lyme disease. N. Engl. J. Med.,  1989, 321(9), 586-596.
[http://dx.doi.org/10.1056/NEJM198908313210906] [PMID: 2668764] 
[3] 
Mead, P.S. Epidemiology of Lyme disease. Infect. Dis. Clin. North Am.,  2015, 29(2), 187-210.
[http://dx.doi.org/10.1016/j.idc.2015.02.010] [PMID: 25999219] 
[4] 
Hinckley, A.F.; Connally, N.P.; Meek, J.I.; Johnson, B.J.; Kemperman, M.M.; Feldman, K.A.; White, J.L.; Mead, P.S. Lyme disease testing by large commercial laboratories in the United States. Clin. Infect. Dis.,  2014, 59(5), 676-681.
[http://dx.doi.org/10.1093/cid/ciu397] [PMID: 24879782] 
[5] 
Pal, U.; Wang, P.; Bao, F.; Yang, X.; Samanta, S.; Schoen, R.; Wormser, G.P.; Schwartz, I.; Fikrig, E. Borrelia burgdorferi basic membrane proteins A and B participate in the genesis of Lyme arthritis. J. Exp. Med.,  2008, 205(1), 133-141.
[http://dx.doi.org/10.1084/jem.20070962] [PMID: 18166585] 
[6] 
Ramamoorthi, N.; Narasimhan, S.; Pal, U.; Bao, F.; Yang, X.F.; Fish, D.; Anguita, J.; Norgard, M.V.; Kantor, F.S.; Anderson, J.F.; Koski, R.A.; Fikrig, E. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature,  2005, 436(7050), 573-577.
[http://dx.doi.org/10.1038/nature03812] [PMID: 16049492] 
[7] 
Aberer, E. Lyme borreliosis--an update. J. Dtsch. Dermatol. Ges.,  2007, 5(5), 406-414.
[http://dx.doi.org/10.1111/j.1610-0387.2007.06285.x] [PMID: 17451386] 
[8] 
Jensenius, M.; Parola, P.; Raoult, D. Threats to international travellers posed by tick-borne diseases. Travel Med. Infect. Dis.,  2006, 4(1), 4-13.
[http://dx.doi.org/10.1016/j.tmaid.2004.11.003] [PMID: 16887719] 
[9] 
Fraser, C.M.; Casjens, S.; Huang, W.M.; Sutton, G.G.; Clayton, R.; Lathigra, R.; White, O.; Ketchum, K.A.; Dodson, R.; Hickey, E.K.; Gwinn, M.; Dougherty, B.; Tomb, J.F.; Fleischmann, R.D.; Richardson, D.; Peterson, J.; Kerlavage, A.R.; Quackenbush, J.; Salzberg, S.; Hanson, M.; van Vugt, R.; Palmer, N.; Adams, M.D.; Gocayne, J.; Weidman, J.; Utterback, T.; Watthey, L.; McDonald, L.; Artiach, P.; Bowman, C.; Garland, S.; Fuji, C.; Cotton, M.D.; Horst, K.; Roberts, K.; Hatch, B.; Smith, H.O.; Venter, J.C. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature,  1997, 390(6660), 580-586.
[http://dx.doi.org/10.1038/37551] [PMID: 9403685] 
[10] 
von Lackum, K.; Stevenson, B. Carbohydrate utilization by the Lyme borreliosis spirochete, Borrelia burgdorferi. FEMS Microbiol. Lett.,  2005, 243(1), 173-179.
[http://dx.doi.org/10.1016/j.femsle.2004.12.002] [PMID: 15668016] 
[11] 
Corona, A.; Schwartz, I. Borrelia burgdorferi: carbon metabolism and the tick-mammal enzootic cycle. Microbiol. Spectr.,  2015, 3(3), 3.
[http://dx.doi.org/10.1128/microbiolspec.MBP-0011-2014] [PMID: 26185064] 
[12] 
Pal, U.; Li, X.; Wang, T.; Montgomery, R.R.; Ramamoorthi, N.; Desilva, A.M.; Bao, F.; Yang, X.; Pypaert, M.; Pradhan, D.; Kantor, F.S.; Telford, S.; Anderson, J.F.; Fikrig, E. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell,  2004, 119(4), 457-468.
[http://dx.doi.org/10.1016/j.cell.2004.10.027] [PMID: 15537536] 
[13] 
Fikrig, E.; Telford, S.R., III; Barthold, S.W.; Kantor, F.S.; Spielman, A.; Flavell, R.A. Elimination of Borrelia burgdorferi from vector ticks feeding on OspA-immunized mice. Proc. Natl. Acad. Sci. USA,  1992, 89(12), 5418-5421.
[http://dx.doi.org/10.1073/pnas.89.12.5418] [PMID: 1608951] 
[14] 
Narasimhan, S.; Santiago, F.; Koski, R.A.; Brei, B.; Anderson, J.F.; Fish, D.; Fikrig, E. Examination of the Borrelia burgdorferi transcriptome in Ixodes scapularis during feeding. J. Bacteriol.,  2002, 184(11), 3122-3125.
[http://dx.doi.org/10.1128/JB.184.11.3122-3125.2002] [PMID: 12003955] 
[15] 
Pal, U.; Fikrig, E. Adaptation of Borrelia burgdorferi in the vector and vertebrate host. Microbes Infect.,  2003, 5(7), 659-666.
[http://dx.doi.org/10.1016/S1286-4579(03)00097-2] [PMID: 12787742] 
[16] 
Boeuf, A.; Schnell, G.; Bernard, Q.; Kern, A.; Westermann, B.; Ehret-Sabatier, L.; Grillon, A.; Schramm, F.; Jaulhac, B.; Boulanger, N. Dissociating effect of salivary gland extract from Ixodes ricinus on human fibroblasts: Potential impact on Borrelia transmission. Ticks Tick Borne Dis.,  2019, 10(2), 433-441.
[http://dx.doi.org/10.1016/j.ttbdis.2018.12.005] [PMID: 30595500] 
[17] 
Cotté, V.; Sabatier, L.; Schnell, G.; Carmi-Leroy, A.; Rousselle, J-C.; Arsène-Ploetze, F.; Malandrin, L.; Sertour, N.; Namane, A.; Ferquel, E.; Choumet, V. Differential expression of Ixodes ricinus salivary gland proteins in the presence of the Borrelia burgdorferi sensu lato complex. J. Proteomics,  2014, 96, 29-43.
[http://dx.doi.org/10.1016/j.jprot.2013.10.033] [PMID: 24189444] 
[18] 
Steere, A.C.; Strle, F.; Wormser, G.P.; Hu, L.T.; Branda, J.A.; Hovius, J.W.R.; Li, X.; Mead, P.S. Lyme borreliosis. Nat. Rev. Dis. Primers,  2016, 2, 16090.
[http://dx.doi.org/10.1038/nrdp.2016.90] [PMID: 27976670] 
[19] 
Anguita, J.; Ramamoorthi, N.; Hovius, J.W.R.; Das, S.; Thomas, V.; Persinski, R.; Conze, D.; Askenase, P.W.; Rincón, M.; Kantor, F.S.; Fikrig, E. Salp15, an ixodes scapularis salivary protein, inhibits CD4(+) T cell activation. Immunity,  2002, 16(6), 849-859.
[http://dx.doi.org/10.1016/S1074-7613(02)00325-4] [PMID: 12121666] 
[20] 
Tyson, K.; Elkins, C.; Patterson, H.; Fikrig, E.; de Silva, A. Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway. Insect Mol. Biol.,  2007, 16(4), 469-479.
[http://dx.doi.org/10.1111/j.1365-2583.2007.00742.x] [PMID: 17651236] 
[21] 
Valenzuela, J.G.; Charlab, R.; Mather, T.N.; Ribeiro, J.M. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J. Biol. Chem.,  2000, 275(25), 18717-18723.
[http://dx.doi.org/10.1074/jbc.M001486200] [PMID: 10749868] 
[22] 
Daix, V.; Schroeder, H.; Praet, N.; Georgin, J.P.; Chiappino, I.; Gillet, L.; de Fays, K.; Decrem, Y.; Leboulle, G.; Godfroid, E.; Bollen, A.; Pastoret, P.P.; Gern, L.; Sharp, P.M.; Vanderplasschen, A. Ixodes ticks belonging to the Ixodes ricinus complex encode a family of anticomplement proteins. Insect Mol. Biol.,  2007, 16(2), 155-166.
[http://dx.doi.org/10.1111/j.1365-2583.2006.00710.x] [PMID: 17298559] 
[23] 
Bernard, Q.; Gallo, R.L.; Jaulhac, B.; Nakatsuji, T.; Luft, B.; Yang, X.; Boulanger, N. Ixodes tick saliva suppresses the keratinocyte cytokine response to TLR2/TLR3 ligands during early exposure to Lyme borreliosis. Exp. Dermatol.,  2016, 25(1), 26-31.
[http://dx.doi.org/10.1111/exd.12853] [PMID: 26307945] 
[24] 
Dai, J.; Narasimhan, S.; Zhang, L.; Liu, L.; Wang, P.; Fikrig, E. Tick histamine release factor is critical for Ixodes scapularis engorgement and transmission of the lyme disease agent. PLoS Pathog.,  2010, 6(11), e1001205
[http://dx.doi.org/10.1371/journal.ppat.1001205] [PMID: 21124826] 
[25] 
Schuijt, T.J.; Coumou, J.; Narasimhan, S.; Dai, J.; Deponte, K.; Wouters, D.; Brouwer, M.; Oei, A.; Roelofs, J.J.; van Dam, A.P.; van der Poll, T.; Van’t Veer, C.; Hovius, J.W.; Fikrig, E. A tick mannose-binding lectin inhibitor interferes with the vertebrate complement cascade to enhance transmission of the lyme disease agent. Cell Host Microbe,  2011, 10(2), 136-146.
[http://dx.doi.org/10.1016/j.chom.2011.06.010] [PMID: 21843870] 
[26] 
Norris, S.J. Antigenic variation with a twist--the Borrelia story. Mol. Microbiol.,  2006, 60(6), 1319-1322.
[http://dx.doi.org/10.1111/j.1365-2958.2006.05204.x] [PMID: 16796669] 
[27] 
Cassatt, D.R.; Patel, N.K.; Ulbrandt, N.D.; Hanson, M.S. DbpA, but not OspA, is expressed by Borrelia burgdorferi during spirochetemia and is a target for protective antibodies. Infect. Immun.,  1998, 66(11), 5379-5387.
[PMID: 9784547] 
[28] 
Ohnishi, J.; Piesman, J.; de Silva, A.M. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc. Natl. Acad. Sci. USA,  2001, 98(2), 670-675.
[http://dx.doi.org/10.1073/pnas.98.2.670] [PMID: 11209063] 
[29] 
de Taeye, S.W.; Kreuk, L.; van Dam, A.P.; Hovius, J.W.; Schuijt, T.J. Complement evasion by Borrelia burgdorferi: it takes three to tango. Trends Parasitol.,  2013, 29(3), 119-128.
[http://dx.doi.org/10.1016/j.pt.2012.12.001] [PMID: 23298533] 
[30] 
Kraiczy, P.; Stevenson, B. Complement regulator-acquiring surface proteins of Borrelia burgdorferi: Structure, function and regulation of gene expression. Ticks Tick Borne Dis.,  2013, 4(1-2), 26-34.
[http://dx.doi.org/10.1016/j.ttbdis.2012.10.039] [PMID: 23219363] 
[31] 
Meri, T.; Amdahl, H.; Lehtinen, M.J.; Hyvärinen, S.; McDowell, J.V.; Bhattacharjee, A.; Meri, S.; Marconi, R.; Goldman, A.; Jokiranta, T.S. Microbes bind complement inhibitor factor H via a common site. PLoS Pathog.,  2013, 9(4), e1003308
[http://dx.doi.org/10.1371/journal.ppat.1003308] [PMID: 23637600] 
[32] 
Pietikäinen, J.; Meri, T.; Blom, A.M.; Meri, S. Binding of the complement inhibitor C4b-binding protein to Lyme disease Borreliae. Mol. Immunol.,  2010, 47(6), 1299-1305.
[http://dx.doi.org/10.1016/j.molimm.2009.11.028] [PMID: 20022381] 
[33] 
Garcia, B.L.; Zhi, H.; Wager, B.; Höök, M.; Skare, J.T. Borrelia burgdorferi BBK32 inhibits the classical pathway by blocking activation of the C1 complement complex. PLoS Pathog.,  2016, 12(1), e1005404
[http://dx.doi.org/10.1371/journal.ppat.1005404] [PMID: 26808924] 
[34] 
Caine, J.A.; Lin, Y.P.; Kessler, J.R.; Sato, H.; Leong, J.M.; Coburn, J. Borrelia burgdorferi outer surface protein C (OspC) binds complement component C4b and confers bloodstream survival. Cell. Microbiol.,  2017, 19(12), 12.
[http://dx.doi.org/10.1111/cmi.12786] [PMID: 28873507] 
[35] 
Müllegger, R.R.; McHugh, G.; Ruthazer, R.; Binder, B.; Kerl, H.; Steere, A.C. Differential expression of cytokine mRNA in skin specimens from patients with erythema migrans or acrodermatitis chronica atrophicans. J. Invest. Dermatol.,  2000, 115(6), 1115-1123.
[http://dx.doi.org/10.1046/j.1523-1747.2000.00198.x] [PMID: 11121150] 
[36] 
Sjöwall, J.; Fryland, L.; Nordberg, M.; Sjögren, F.; Garpmo, U.; Jansson, C.; Carlsson, S.A.; Bergström, S.; Ernerudh, J.; Nyman, D.; Forsberg, P.; Ekerfelt, C. Decreased Th1-type inflammatory cytokine expression in the skin is associated with persisting symptoms after treatment of erythema migrans. PLoS One,  2011, 6(3), e18220
[http://dx.doi.org/10.1371/journal.pone.0018220] [PMID: 21483819] 
[37] 
Giambartolomei, G.H.; Dennis, V.A.; Philipp, M.T. Borrelia burgdorferi stimulates the production of interleukin-10 in peripheral blood mononuclear cells from uninfected humans and rhesus monkeys. Infect. Immun.,  1998, 66(6), 2691-2697.
[PMID: 9596735] 
[38] 
Lazarus, J.J.; Meadows, M.J.; Lintner, R.E.; Wooten, R.M. IL-10 deficiency promotes increased Borrelia burgdorferi clearance predominantly through enhanced innate immune responses. J. Immunol.,  2006, 177(10), 7076-7085.
[http://dx.doi.org/10.4049/jimmunol.177.10.7076] [PMID: 17082624] 
[39] 
Embers, M.E.; Ramamoorthy, R.; Philipp, M.T. Survival strategies of Borrelia burgdorferi, the etiologic agent of Lyme disease. Microbes Infect.,  2004, 6(3), 312-318.
[http://dx.doi.org/10.1016/j.micinf.2003.11.014] [PMID: 15065567] 
[40] 
Schutzer, S.E.; Coyle, P.K.; Reid, P.; Holland, B. Borrelia burgdorferi-specific immune complexes in acute Lyme disease. JAMA,  1999, 282(20), 1942-1946.
[http://dx.doi.org/10.1001/jama.282.20.1942] [PMID: 10580460] 
[41] 
Coyle, P.K.; Schutzer, S.E.; Belman, A.L.; Krupp, L.B.; Golightly, M.G. Cerebrospinal fluid immune complexes in patients exposed to Borrelia burgdorferi: detection of Borrelia-specific and -nonspecific complexes. Ann. Neurol.,  1990, 28(6), 739-744.
[http://dx.doi.org/10.1002/ana.410280603] [PMID: 2285261] 
[42] 
Blevins, J.S.; Hagman, K.E.; Norgard, M.V. Assessment of decorin-binding protein A to the infectivity of Borrelia burgdorferi in the murine models of needle and tick infection. BMC Microbiol.,  2008, 8, 82.
[http://dx.doi.org/10.1186/1471-2180-8-82] [PMID: 18507835] 
[43] 
Brown, E.L.; Wooten, R.M.; Johnson, B.J.; Iozzo, R.V.; Smith, A.; Dolan, M.C.; Guo, B.P.; Weis, J.J.; Höök, M. Resistance to Lyme disease in decorin-deficient mice. J. Clin. Invest.,  2001, 107(7), 845-852.
[http://dx.doi.org/10.1172/JCI11692] [PMID: 11285303] 
[44] 
Caimano, M.J.; Eggers, C.H.; Hazlett, K.R.; Radolf, J.D. RpoS is not central to the general stress response in Borrelia burgdorferi but does control expression of one or more essential virulence determinants. Infect. Immun.,  2004, 72(11), 6433-6445.
[http://dx.doi.org/10.1128/IAI.72.11.6433-6445.2004] [PMID: 15501774] 
[45] 
Guo, B.P.; Brown, E.L.; Dorward, D.W.; Rosenberg, L.C.; Höök, M. Decorin-binding adhesins from Borrelia burgdorferi. Mol. Microbiol.,  1998, 30(4), 711-723.
[http://dx.doi.org/10.1046/j.1365-2958.1998.01103.x] [PMID: 10094620] 
[46] 
Hyde, J.A.; Weening, E.H.; Chang, M.; Trzeciakowski, J.P.; Höök, M.; Cirillo, J.D.; Skare, J.T. Bioluminescent imaging of Borrelia burgdorferi in vivo demonstrates that the fibronectin-binding protein BBK32 is required for optimal infectivity. Mol. Microbiol.,  2011, 82(1), 99-113.
[http://dx.doi.org/10.1111/j.1365-2958.2011.07801.x] [PMID: 21854463] 
[47] 
Lin, Y.P.; Benoit, V.; Yang, X.; Martínez-Herranz, R.; Pal, U.; Leong, J.M. Strain-specific variation of the decorin-binding adhesin DbpA influences the tissue tropism of the lyme disease spirochete. PLoS Pathog.,  2014, 10(7), e1004238
[http://dx.doi.org/10.1371/journal.ppat.1004238] [PMID: 25079227] 
[48] 
Shi, Y.; Xu, Q.; McShan, K.; Liang, F.T. Both decorin-binding proteins A and B are critical for the overall virulence of Borrelia burgdorferi. Infect. Immun.,  2008, 76(3), 1239-1246.
[http://dx.doi.org/10.1128/IAI.00897-07] [PMID: 18195034] 
[49] 
Weening, E.H.; Parveen, N.; Trzeciakowski, J.P.; Leong, J.M.; Höök, M.; Skare, J.T. Borrelia burgdorferi lacking DbpBA exhibits an early survival defect during experimental infection. Infect. Immun.,  2008, 76(12), 5694-5705.
[http://dx.doi.org/10.1128/IAI.00690-08] [PMID: 18809667] 
[50] 
Brissette, C.A.; Gaultney, R.A. That’s my story, and I’m sticking to it--an update on B. burgdorferi adhesins. Front. Cell. Infect. Microbiol.,  2014, 4, 41.
[http://dx.doi.org/10.3389/fcimb.2014.00041] [PMID: 24772392] 
[51] 
Gaultney, R.A.; Gonzalez, T.; Floden, A.M.; Brissette, C.A. BB0347, from the lyme disease spirochete Borrelia burgdorferi, is surface exposed and interacts with the CS1 heparin-binding domain of human fibronectin. PLoS One,  2013, 8(9), e75643
[http://dx.doi.org/10.1371/journal.pone.0075643] [PMID: 24086600] 
[52] 
Brissette, C.A.; Verma, A.; Bowman, A.; Cooley, A.E.; Stevenson, B. The Borrelia burgdorferi outer-surface protein ErpX binds mammalian laminin. Microbiology,  2009, 155(Pt 3), 863-872.
[http://dx.doi.org/10.1099/mic.0.024604-0] [PMID: 19246757] 
[53] 
Verma, A.; Brissette, C.A.; Bowman, A.; Stevenson, B. Borrelia burgdorferi BmpA is a laminin-binding protein. Infect. Immun.,  2009, 77(11), 4940-4946.
[http://dx.doi.org/10.1128/IAI.01420-08] [PMID: 19703983] 
[54] 
Floden, A.M.; Watt, J.A.; Brissette, C.A. Borrelia burgdorferi enolase is a surface-exposed plasminogen binding protein. PLoS One,  2011, 6(11), e27502
[http://dx.doi.org/10.1371/journal.pone.0027502] [PMID: 22087329] 
[55] 
Fuchs, H.; Wallich, R.; Simon, M.M.; Kramer, M.D. The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin(ogen) receptor. Proc. Natl. Acad. Sci. USA,  1994, 91(26), 12594-12598.
[http://dx.doi.org/10.1073/pnas.91.26.12594] [PMID: 7809084] 
[56] 
Hallström, T.; Haupt, K.; Kraiczy, P.; Hortschansky, P.; Wallich, R.; Skerka, C.; Zipfel, P.F. Complement regulator-acquiring surface protein 1 of Borrelia burgdorferi binds to human bone morphogenic protein 2, several extracellular matrix proteins, and plasminogen. J. Infect. Dis.,  2010, 202(3), 490-498.
[http://dx.doi.org/10.1086/653825] [PMID: 20565259] 
[57] 
Koenigs, A.; Hammerschmidt, C.; Jutras, B.L.; Pogoryelov, D.; Barthel, D.; Skerka, C.; Kugelstadt, D.; Wallich, R.; Stevenson, B.; Zipfel, P.F.; Kraiczy, P. BBA70 of Borrelia burgdorferi is a novel plasminogen-binding protein. J. Biol. Chem.,  2013, 288(35), 25229-25243.
[http://dx.doi.org/10.1074/jbc.M112.413872] [PMID: 23861404] 
[58] 
Lagal, V.; Portnoï, D.; Faure, G.; Postic, D.; Baranton, G. Borrelia burgdorferi sensu stricto invasiveness is correlated with OspC-plasminogen affinity. Microbes Infect.,  2006, 8(3), 645-652.
[http://dx.doi.org/10.1016/j.micinf.2005.08.017] [PMID: 16513394] 
[59] 
Nogueira, S.V.; Smith, A.A.; Qin, J.H.; Pal, U. A surface enolase participates in Borrelia burgdorferi-plasminogen interaction and contributes to pathogen survival within feeding ticks. Infect. Immun.,  2012, 80(1), 82-90.
[http://dx.doi.org/10.1128/IAI.05671-11] [PMID: 22025510] 
[60] 
Önder, Ö.; Humphrey, P.T.; McOmber, B.; Korobova, F.; Francella, N.; Greenbaum, D.C.; Brisson, D. OspC is potent plasminogen receptor on surface of Borrelia burgdorferi. J. Biol. Chem.,  2012, 287(20), 16860-16868.
[http://dx.doi.org/10.1074/jbc.M111.290775] [PMID: 22433849] 
[61] 
Toledo, A.; Coleman, J.L.; Kuhlow, C.J.; Crowley, J.T.; Benach, J.L. The enolase of Borrelia burgdorferi is a plasminogen receptor released in outer membrane vesicles. Infect. Immun.,  2012, 80(1), 359-368.
[http://dx.doi.org/10.1128/IAI.05836-11] [PMID: 22083700] 
[62] 
Coleman, J.L.; Roemer, E.J.; Benach, J.L. Plasmin-coated borrelia Burgdorferi degrades soluble and insoluble components of the mammalian extracellular matrix. Infect. Immun.,  1999, 67(8), 3929-3936.
[PMID: 10417158] 
[63] 
Behera, A.K.; Durand, E.; Cugini, C.; Antonara, S.; Bourassa, L.; Hildebrand, E.; Hu, L.T.; Coburn, J. Borrelia burgdorferi BBB07 interaction with integrin alpha3beta1 stimulates production of pro-inflammatory mediators in primary human chondrocytes. Cell. Microbiol.,  2008, 10(2), 320-331.
[PMID: 17822440] 
[64] 
Ristow, L.C.; Miller, H.E.; Padmore, L.J.; Chettri, R.; Salzman, N.; Caimano, M.J.; Rosa, P.A.; Coburn, J. The β3-integrin ligand of Borrelia burgdorferi is critical for infection of mice but not ticks. Mol. Microbiol.,  2012, 85(6), 1105-1118.
[http://dx.doi.org/10.1111/j.1365-2958.2012.08160.x] [PMID: 22758390] 
[65] 
Ristow, L.C.; Bonde, M.; Lin, Y.P.; Sato, H.; Curtis, M.; Wesley, E.; Hahn, B.L.; Fang, J.; Wilcox, D.A.; Leong, J.M.; Bergström, S.; Coburn, J. Integrin binding by Borrelia burgdorferi P66 facilitates dissemination but is not required for infectivity. Cell. Microbiol.,  2015, 17(7), 1021-1036.
[http://dx.doi.org/10.1111/cmi.12418] [PMID: 25604835] 
[66] 
Wood, E.; Tamborero, S.; Mingarro, I.; Esteve-Gassent, M.D. BB0172, a Borrelia burgdorferi outer membrane protein that binds integrin α3β1. J. Bacteriol.,  2013, 195(15), 3320-3330.
[http://dx.doi.org/10.1128/JB.00187-13] [PMID: 23687274] 
[67] 
Charon, N.W.; Cockburn, A.; Li, C.; Liu, J.; Miller, K.A.; Miller, M.R.; Motaleb, M.A.; Wolgemuth, C.W. The unique paradigm of spirochete motility and chemotaxis. Annu. Rev. Microbiol.,  2012, 66, 349-370.
[http://dx.doi.org/10.1146/annurev-micro-092611-150145] [PMID: 22994496] 
[68] 
Charon, N.W.; Goldstein, S.F. Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu. Rev. Genet.,  2002, 36, 47-73.
[http://dx.doi.org/10.1146/annurev.genet.36.041602.134359] [PMID: 12429686] 
[69] 
Li, C.; Motaleb, A.; Sal, M.; Goldstein, S.F.; Charon, N.W. Spirochete periplasmic flagella and motility. J. Mol. Microbiol. Biotechnol.,  2000, 2(4), 345-354.
[PMID: 11075905] 
[70] 
Motaleb, M.A.; Liu, J.; Wooten, R.M. Spirochetal motility and chemotaxis in the natural enzootic cycle and development of Lyme disease. Curr. Opin. Microbiol.,  2015, 28, 106-113.
[http://dx.doi.org/10.1016/j.mib.2015.09.006] [PMID: 26519910] 
[71] 
Motaleb, M.A.; Miller, M.R.; Bakker, R.G.; Li, C.; Charon, N.W. Isolation and characterization of chemotaxis mutants of the Lyme disease Spirochete Borrelia burgdorferi using allelic exchange mutagenesis, flow cytometry, and cell tracking. Methods Enzymol.,  2007, 422, 421-437.
[http://dx.doi.org/10.1016/S0076-6879(06)22021-4] [PMID: 17628152] 
[72] 
Sze, C.W.; Zhang, K.; Kariu, T.; Pal, U.; Li, C. Borrelia burgdorferi needs chemotaxis to establish infection in mammals and to accomplish its enzootic cycle. Infect. Immun.,  2012, 80(7), 2485-2492.
[http://dx.doi.org/10.1128/IAI.00145-12] [PMID: 22508862] 
[73] 
Coulter, P.; Lema, C.; Flayhart, D.; Linhardt, A.S.; Aucott, J.N.; Auwaerter, P.G.; Dumler, J.S. Two-year evaluation of Borrelia burgdorferi culture and supplemental tests for definitive diagnosis of Lyme disease. J. Clin. Microbiol.,  2005, 43(10), 5080-5084.
[http://dx.doi.org/10.1128/JCM.43.10.5080-5084.2005] [PMID: 16207966] 
[74] 
Wormser, G.P.; McKenna, D.; Carlin, J.; Nadelman, R.B.; Cavaliere, L.F.; Holmgren, D.; Byrne, D.W.; Nowakowski, J. Brief communication: hematogenous dissemination in early Lyme disease. Ann. Intern. Med.,  2005, 142(9), 751-755.
[http://dx.doi.org/10.7326/0003-4819-142-9-200505030-00011] [PMID: 15867407] 
[75] 
Shapiro, E.D. Clinical practice. Lyme disease. N. Engl. J. Med.,  2014, 370(18), 1724-1731.
[http://dx.doi.org/10.1056/NEJMcp1314325] [PMID: 24785207] 
[76] 
Meta-Analysis, A. J. Interferon Cytokine Res.,  2017, 37(10), 433-439.Yang.; J Han, X.; Liu, A.; Bao, F.; Peng, Y.; Tao, L.; Ma, M.;
Bai, R.; Dai, X..  Chemokine CXC Ligand 13 in Cerebrospinal Fluid Can Be Used as an Early Diagnostic Biomarker for Lyme Neuroborreliosis
[http://dx.doi.org/10.1089/jir.2016.0101] [PMID: 28972436] 
[77] 
Rupprecht, T.A.; Pfister, H.W.; Angele, B.; Kastenbauer, S.; Wilske, B.; Koedel, U. The chemokine CXCL13 (BLC): a putative diagnostic marker for neuroborreliosis. Neurology,  2005, 65(3), 448-450.
[http://dx.doi.org/10.1212/01.wnl.0000171349.06645.79] [PMID: 16087912] 
[78] 
Rupprecht, T.A.; Kirschning, C.J.; Popp, B.; Kastenbauer, S.; Fingerle, V.; Pfister, H.W.; Koedel, U. Borrelia garinii induces CXCL13 production in human monocytes through Toll-like receptor 2. Infect. Immun.,  2007, 75(9), 4351-4356.
[http://dx.doi.org/10.1128/IAI.01642-06] [PMID: 17562761] 
[79] 
Cepok, S.; Zhou, D.; Vogel, F.; Rosche, B.; Grummel, V.; Sommer, N.; Hemmer, B. The immune response at onset and during recovery from Borrelia burgdorferi meningoradiculitis. Arch. Neurol.,  2003, 60(6), 849-855.
[http://dx.doi.org/10.1001/archneur.60.6.849] [PMID: 12810490] 
[80] 
Tatro, J.B.; Romero, L.I.; Beasley, D.; Steere, A.C.; Reichlin, S. Borrelia burgdorferi and Escherichia coli lipopolysaccharides induce nitric oxide and interleukin-6 production in cultured rat brain cells. J. Infect. Dis.,  1994, 169(5), 1014-1022.
[http://dx.doi.org/10.1093/infdis/169.5.1014] [PMID: 7513330] 
[81] 
Grusell, M.; Widhe, M.; Ekerfelt, C. Increased expression of the Th1-inducing cytokines interleukin-12 and interleukin-18 in cerebrospinal fluid but not in sera from patients with Lyme neuroborreliosis. J. Neuroimmunol.,  2002, 131(1-2), 173-178.
[http://dx.doi.org/10.1016/S0165-5728(02)00255-2] [PMID: 12458049] 
[82] 
Widhe, M.; Jarefors, S.; Ekerfelt, C.; Vrethem, M.; Bergstrom, S.; Forsberg, P.; Ernerudh, J. Borrelia-specific interferon-gamma and interleukin-4 secretion in cerebrospinal fluid and blood during Lyme borreliosis in humans: association with clinical outcome. J. Infect. Dis.,  2004, 189(10), 1881-1891.
[http://dx.doi.org/10.1086/382893] [PMID: 15122525] 
[83] 
Weller, M.; Stevens, A.; Sommer, N.; Wiethölter, H.; Dichgans, J. Cerebrospinal fluid interleukins, immunoglobulins, and fibronectin in neuroborreliosis. Arch. Neurol.,  1991, 48(8), 837-841.
[http://dx.doi.org/10.1001/archneur.1991.00530200079022] [PMID: 1898258] 
[84] 
Cepok, S.; Rosche, B.; Grummel, V.; Vogel, F.; Zhou, D.; Sayn, J.; Sommer, N.; Hartung, H.P.; Hemmer, B. Short-lived plasma blasts are the main B cell effector subset during the course of multiple sclerosis. Brain,  2005, 128(Pt 7), 1667-1676.
[http://dx.doi.org/10.1093/brain/awh486] [PMID: 15800022] 
[85] 
Brandes, M.; Legler, D.F.; Spoerri, B.; Schaerli, P.; Moser, B. Activation-dependent modulation of B lymphocyte migration to chemokines. Int. Immunol.,  2000, 12(9), 1285-1292.
[http://dx.doi.org/10.1093/intimm/12.9.1285] [PMID: 10967023] 
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DOI https://dx.doi.org/10.2174/1389203720666191015145714	Print ISSN 1389-2037
Publisher Name Bentham Science Publisher	Online ISSN 1875-5550
Current Protein & Peptide Science

Molecular Interactions During Borrelia burgdorferi Migration from the Vector to the Mammalian Nervous System

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