Streptococcal Collagen-like Protein 1 Binds Wound Fibronectin: Implications in Pathogen Targeting

Author(s): Dudley H. McNitt, Livingston Van De Water, Daniela Marasco, Rita Berisio, Slawomir Lukomski*.

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 11 , 2019

  Journal Home
Translate in Chinese


Group A Streptococcus (GAS) infections are responsible for significant morbidity and mortality worldwide. The outlook for an effective global vaccine is reduced because of significant antigenic variation among GAS strains worldwide. Other challenges in GAS therapy include the lack of common access to antibiotics in developing countries, as well as allergy to and treatment failures with penicillin and increasing erythromycin resistance in the industrialized world. At the portal of entry, GAS binds to newly deposited extracellular matrix, which is rich in cellular fibronectin isoforms with extra domain A (EDA, also termed EIIIA) via the surface adhesin, the streptococcal collagen-like protein 1 (Scl1). Recombinant Scl1 constructs, derived from diverse GAS strains, bind the EDA loop segment situated between the C and C’ β-strands. Despite the sequence diversity in Scl1 proteins, multiple sequence alignments and secondary structure predictions of Scl1 variants, as well as crystallography and homology modeling studies, point to a conserved mechanism of Scl1-EDA binding. We propose that targeting this interaction may prevent the progression of infection. A synthetic cyclic peptide, derived from the EDA C-C’ loop, binds to recombinant Scl1 with a micromolar dissociation constant. This review highlights the current concept of EDA binding to Scl1 and provides incentives to exploit this binding to treat GAS infections and wound colonization.

Keywords: Scl1, adhesins, group A Streptococcus colonization, EDA fibronectin, wound microenvironment, pathogen.

Strimbu, K.; Tavel, J.A. What are biomarkers? Curr. Opin. HIV AIDS, 2010, 5(6), 463-466.
Hsueh, C.T.; Liu, D.; Wang, H. Novel biomarkers for diagnosis, prognosis, targeted therapy and clinical trials. Biomark. Res., 2013, 1, 1.
Squeglia, F.; Ruggiero, A.; De Simone, A.; Berisio, R. A structural overview of mycobacterial adhesins: Key biomarkers for diagnostics and therapeutics. Protein Sci., 2018, 27(2), 369-380.
Durighello, E.; Bellanger, L.; Ezan, E.; Armengaud, J. Proteogenomic biomarkers for identification of Francisella species and subspecies by matrix-assisted laser desorption ionization-time-of-flight mass spectrometry. Anal. Chem., 2014, 86(19), 9394-9398.
Bachert, B.A.; Choi, S.J.; Snyder, A.K.; Rio, R.V.M.; Durney, B.C.; Holland, L.A.; Amemiya, K.; Welkos, S.L.; Bozue, J.A.; Cote, C.K.; Berisio, R.; Lukomski, S. A unique set of the Burkholderia collagen-like proteins provides insight into pathogenesis, genome evolution and niche adaptation, and infection detection. PLoS One, 2015, 10(9)e0137578
Solomon, S.L.; Oliver, K.B. Antibiotic resistance threats in the United States: Stepping back from the brink. Am. Fam. Physician, 2014, 89(12), 938-941.
Carapetis, J.R.; Steer, A.C.; Mulholland, E.K.; Weber, M. The global burden of group A streptococcal diseases. Lancet Infect. Dis., 2005, 5(11), 685-694.
Bisno, A.L.; Pearce, I.A.; Wall, H.P.; Moody, M.D.; Stollerman, G.H. Contrasting epidemiology of acute rheumatic fever and acute glomerulonephritis. N. Engl. J. Med., 1970, 283(11), 561-565.
Swedo, S.E.; Leonard, H.L.; Mittleman, B.B.; Allen, A.J.; Rapoport, J.L.; Dow, S.P.; Kanter, M.E.; Chapman, F.; Zabriskie, J. Identification of children with pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections by a marker associated with rheumatic fever. Am. J. Psychiatry, 1997, 154(1), 110-112.
Cunningham, M.W. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev., 2000, 13(3), 470-511.
Bessen, D.E.; Lizano, S. Tissue tropisms in group A streptococcal infections. Future Microbiol., 2010, 5(4), 623-638.
Fischetti, V. In Streptococcus pyogenes : Basic Biology to Clinical Manifestations; Ferretti JJ, S.D., Fischetti VA, Ed.; Univeristy of Oklahoma. Oklahoma City, OK,, 2016.
Sanderson-Smith, M.; De Oliveira, D.M.; Guglielmini, J.; McMillan, D.J.; Vu, T.; Holien, J.K.; Henningham, A.; Steer, A.C.; Bessen, D.E.; Dale, J.B.; Curtis, N.; Beall, B.W.; Walker, M.J.; Parker, M.W.; Carapetis, J.R.; Van Melderen, L.; Sriprakash, K.S.; Smeesters, P.R. A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J. Infect. Dis., 2014, 210(8), 1325-1338.
Rasmussen, M.; Edén, A.; Björck, L. SclA, a novel collagen-like surface protein of Streptococcus pyogenes. Infect. Immun., 2000, 68(11), 6370-6377.
Lukomski, S.; Nakashima, K.; Abdi, I.; Cipriano, V.J.; Shelvin, B.J.; Graviss, E.A.; Musser, J.M. Identification and characterization of a second extracellular collagen-like protein made by group A Streptococcus: control of production at the level of translation. Infect. Immun., 2001, 69(3), 1729-1738.
Rasmussen, M.; Björck, L. Unique regulation of SclB - a novel collagen-like surface protein of Streptococcus pyogenes. Mol. Microbiol., 2001, 40(6), 1427-1438.
Whatmore, A.M. Streptococcus pyogenes sclB encodes a putative hypervariable surface protein with a collagen-like repetitive structure. Microbiology, 2001, 147(Pt 2), 419-429.
Lukomski, S.; Nakashima, K.; Abdi, I.; Cipriano, V.J.; Ireland, R.M.; Reid, S.D.; Adams, G.G.; Musser, J.M. Identification and characterization of the scl gene encoding a group A Streptococcus extracellular protein virulence factor with similarity to human collagen. Infect. Immun., 2000, 68(12), 6542-6553.
Caswell, C.C.; Oliver-Kozup, H.; Han, R.; Lukomska, E.; Lukomski, S. Scl1, the multifunctional adhesin of group A Streptococcus, selectively binds cellular fibronectin and laminin, and mediates pathogen internalization by human cells. FEMS Microbiol. Lett., 2010, 303(1), 61-68.
Oliver-Kozup, H.A.; Elliott, M.; Bachert, B.A.; Martin, K.H.; Reid, S.D.; Schwegler-Berry, D.E.; Green, B.J.; Lukomski, S. The streptococcal collagen-like protein-1 (Scl1) is a significant determinant for biofilm formation by group A Streptococcus. BMC Microbiol., 2011, 11, 262.
Oliver-Kozup, H.; Martin, K.H.; Schwegler-Berry, D.; Green, B.J.; Betts, C.; Shinde, A.V.; Van De Water, L.; Lukomski, S. The group A streptococcal collagen-like protein-1, Scl1, mediates biofilm formation by targeting the extra domain A-containing variant of cellular fibronectin expressed in wounded tissue. Mol. Microbiol., 2013, 87(3), 672-689.
Lancefield, R.C. A serological differnentation of human and other groups of hemolytic streptococci. J. Exp. Med., 1933, 57(4), 571-595.
Steed, L.L.; Korgenski, E.K.; Daly, J.A. Rapid detection of Streptococcus pyogenes in pediatric patient specimens by DNA probe. J. Clin. Microbiol., 1993, 31(11), 2996-3000.
Anderson, N.W.; Buchan, B.W.; Mayne, D.; Mortensen, J.E.; Mackey, T-L.A.; Ledeboer, N.A. Multicenter clinical evaluation of the illumigene group A Streptococcus DNA amplification assay for detection of group A Streptococcus from pharyngeal swabs. J. Clin. Microbiol., 2013, 51(5), 1474-1477.
Spellerberg, B.; Brandt, C. In: Streptococcus pyogenes : Basic Biology to Clinical Manifestations. Ferretti JJ, S.D., Fischetti VA, Ed.; University of Oklahoma Health Sciences Center: Internet,, 2016.
Sumby, P.; Whitney, A.R.; Graviss, E.A.; DeLeo, F.R.; Musser, J.M. Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog., 2006, 2(1)e5
Almengor, A.C.; McIver, K.S. Transcriptional activation of sclA by Mga requires a distal binding site in Streptococcus pyogenes. J. Bacteriol., 2004, 186(23), 7847-7857.
Spanier, J.G.; Jones, S.J.; Cleary, P. Small DNA deletions creating avirulence in Streptococcus pyogenes. Science, 1984, 225(4665), 935-938.
Podbielski, A. Ubiquitous occurrence of virR and scpA genes in group A streptococci. Med. Microbiol. Immunol., 1992, 181(4), 227-240.
Scott, J.R.; Cleary, P.; Caparon, M.G.; Heden, K.M.L.; Musser, J.M.; Hollingshead, S.; Podbielski, A. New name for the positive regulator of the M protein of group A Streptococcus. Mol. Microbiol., 1995, 17(4), 799.
Bessen, D.; Manoharan, A.; Luo, F.; Wertz, J.; Robinson, D. Evolution of transcription regulatory genes is linked to niche specialization in the bacterial pathogen Streptococcus pyogenes. J. Bacteriol., 2005, 187(12), 4163-4172.
Caparon, M.G.; Scott, J.R. Identification of a gene that regulates expression of M protein, the major virulence determinant of group A streptococci. Proc. Natl. Acad. Sci. USA, 1987, 84(23), 8677-8681.
Hoe, N.P.; Nakashima, K.; Lukomski, S.; Grigsby, D.; Liu, M.; Kordari, P.; Dou, S-J.; Pan, X.; Vuopio-Varkila, J.; Salmenlinna, S.; McGeer, A.; Low, D.E.; Schwartz, B.; Schuchat, A.; Naidich, S.; De Lorenzo, D.; Fu, Y-X.; Musser, J.M. Rapid selection of complement-inhibiting protein variants in group A Streptococcus epidemic waves. Nat. Med., 1999, 5(8), 924-929.
Podbielski, A. Three different types of organization of the vir regulon in group A streptococci. Mol. Gen. Genet., 1993, 237(1-2), 287-300.
Tsatsaronis, J.A.; Hollands, A.; Cole, J.N.; Maamary, P.G.; Gillen, C.M.; Ben Zakour, N.L.; Kotb, M.; Nizet, V.; Beatson, S.A.; Walker, M.J.; Sanderson-Smith, M.L. Streptococcal collagen-like protein A and general stress protein 24 are immunomodulating virulence factors of group A Streptococcus. FASEB J., 2013, 27(7), 2633-2643.
Cole, J.N.; Ramirez, R.D.; Currie, B.J.; Cordwell, S.J.; Djordjevic, S.P.; Walker, M.J. Surface analyses and immune reactivities of major cell wall-associated proteins of group A Streptococcus. Infect. Immun., 2005, 73(5), 3137-3146.
Stevens, D.L.; Tanner, M.H.; Winship, J. Reappearance of scarlet fever toxin A among streptococci in the Rocky Mountain West: severe group A streptococcal infections associated with a toxic shock-like syndrome. N. Engl. J. Med., 1989, 321(1), 1-7.
Musser, J.M.; Hauser, A.R.; Kim, M.H.; Schlievert, P.M.; Nelson, K.; Selander, R.K. Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: Clonal diversity and pyrogenic exotoxin expression. Proc. Natl. Acad. Sci. USA, 1991, 88(7), 2668-2672.
Cleary, P.P.; Kaplan, E.L.; Handley, J.P.; Wlazlo, A.; Kim, M.H.; Hauser, A.R.; Schlievert, P.M. Clonal basis for resurgence of serious Streptococcus pyogenes disease in the 1980s. Lancet, 1992, 339(8792), 518-521.
Bachert, B.A.; Choi, S.J.; LaSala, P.R.; Harper, T.I.; McNitt, D.H.; Boehm, D.T.; Caswell, C.C.; Ciborowski, P.; Keene, D.R.; Flores, A.R.; Musser, J.M.; Squeglia, F.; Marasco, D.; Berisio, R.; Lukomski, S. Unique footprint in the scl1.3 locus affects adhesion and biofilm formation of the invasive M3-type group A Streptococcus. Front. Cell. Infect. Microbiol., 2016, 6, 90.
Sumby, P.; Porcella, S.; Madrigal, A.; Barbian, K.; Virtaneva, K.; Ricklefs, S.; Sturdevant, D.; Graham, M.; Vuopio-Varkila, J.; Hoe, N.; Musser, J. Evolutionary origin and emergence of a highly successful clone of serotype M1 group A Streptococcus involved multiple horizontal gene transfer events. J. Infect. Dis., 2005, 192(5), 771-782.
Aziz, R.; Kotb, M. Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg. Infect. Dis., 2008, 14(10), 1511-1517.
Green, N.M.; Beres, S.B.; Graviss, E.A.; Allison, J.E.; McGeer, A.J.; Vuopio-Varkila, J.; LeFebvre, R.B.; Musser, J.M. Genetic diversity among type emm28 group A Streptococcus strains causing invasive infections and pharyngitis. J. Clin. Microbiol., 2005, 43(8), 4083-4091.
Stevens, D.L.; Kaplan, E.L., Eds.; Streptococcal infections: clinical aspects, microbiology, and molecular pathogenesis; Oxford University Press: New York, N.Y., 2000.
Chuang, I.; Van Beneden, C.; Beall, B.; Schuchat, A. Population-based surveillance for postpartum invasive group a Streptococcus infections, 1995-2000. Clin. Infect. Dis., 2002, 35(6), 665-670.
Gaworzewska, E.; Colman, G. Changes in the pattern of infection caused by Streptococcus pyogenes. Epidemiol. Infect., 1988, 100(2), 257-269.
Eriksson, B.K.; Norgren, M.; McGregor, K.; Spratt, B.G.; Normark, B.H. Group A streptococcal infections in Sweden: a comparative study of invasive and noninvasive infections and analysis of dominant T28 emm28 isolates. Clin. Infect. Dis., 2003, 37(9), 1189-1193.
Shulman, S.T.; Tanz, R.R.; Kabat, W.; Kabat, K.; Cederlund, E.; Patel, D.; Li, Z.; Sakota, V.; Dale, J.B.; Beall, B. Group A streptococcal pharyngitis serotype surveillance in North America, 2000-2002. Clin. Infect. Dis., 2004, 39(3), 325-332.
O’Brien, K.L.; Beall, B.; Barrett, N.L. Epidemiology of invasive group A Streptococcus disease in the United States, 1995-1999. Clin. Infect. Dis., 2002, 35, 268-276.
Hoe, N.; Lukomska, E.; Musser, J.; Lukomski, S. Characterization of the immune response to collagen-like proteins Scl1 and Scl2 of serotype M1 and M28 group A Streptococcus. FEMS Microbiol. Lett., 2007, 277(2), 142-149.
Chaudhary, P.; Kumar, R.; Sagar, V.; Sarkar, S.; Singh, R.; Ghosh, S.; Singh, S.; Chakraborti, A. Assessment of Cpa, Scl1 and Scl2 in clinical group A Streptococcus isolates and patients from north India: An evaluation of the host pathogen interaction. Res. Microbiol., 2018, 169(1), 11-19.
Akesson, P.; Rasmussen, M.; Mascini, E.; von Pawel-Rammingen, U.; Janulczyk, R.; Collin, M.; Olsen, A.; Mattsson, E.; Olsson, M.L.; Bjӧrck, L.; Christensson, B. Low antibody levels against cell wall-attached proteins of Streptococcus pyogenes predispose for severe invasive disease. J. Infect. Dis., 2004, 189, 797-804.
Lukomski, S.; Bachert, B.A.; Squeglia, F.; Berisio, R. Collagen-like proteins of pathogenic streptococci. Mol. Microbiol., 2017, 103(6), 919-930.
Xu, Y.; Keene, D.R.; Bujnicki, J.M.; Höök, M.; Lukomski, S. Streptococcal Scl1 and Scl2 proteins form collagen-like triple helices. J. Biol. Chem., 2002, 277(30), 27312-27318.
Mohs, A.; Silva, T.; Yoshida, T.; Amin, R.; Lukomski, S.; Inouye, M.; Brodsky, B. Mechanism of stabilization of a bacterial collagen triple helix in the absence of hydroxyproline. J. Biol. Chem., 2007, 282(41), 29757-29765.
Okuyama, K. Revisiting the molecular structure of collagen. Connect. Tissue Res., 2008, 49(5), 299-310.
Brodsky, B.; Persikov, A.V. Molecular structure of the collagen triple helix. Adv. Protein Chem., 2005, 70, 301-339.
Shoulders, M.D.; Raines, R.T. Collagen structure and stability. Annu. Rev. Biochem., 2009, 78, 929-958.
Berisio, R.; Vitagliano, L.; Mazzarella, L.; Zagari, A. Crystal structure of the collagen triple helix model [(Pro-Pro-Gly)10]3. Protein Sci., 2002, 11(2), 262-270.
Berisio, R.; Granata, V.; Vitagliano, L.; Zagari, A. Imino acids and collagen triple helix stability: Characterization of collagen-like polypeptides containing Hyp-Hyp-Gly sequence repeats. J. Am. Chem. Soc., 2004, 126(37), 11402-11403.
Berisio, R.; Granata, V.; Vitagliano, L.; Zagari, A. Characterization of collagen-like heterotrimers: Implications for triple-helix stability. Biopolymers, 2004, 73(6), 682-688.
Vitagliano, L.; Berisio, R.; Mastrangelo, A.; Mazzarella, L.; Zagari, A. Preferred proline puckerings in cis and trans peptide groups: Implications for collagen stability. Protein Sci., 2001, 10(12), 2627-2632.
Berisio, R.; De Simone, A.; Ruggiero, A.; Improta, R.; Vitagliano, L. Role of side chains in collagen triple helix stabilization and partner recognition. J. Pept. Sci., 2009, 15(3), 131-140.
Improta, R.; Berisio, R.; Vitagliano, L. Contribution of dipole-dipole interactions to the stability of the collagen triple helix. Protein Sci., 2008, 17(5), 955-961.
Chan, V.C.; Ramshaw, J.A.; Kirkpatrick, A.; Beck, K.; Brodsky, B. Positional preferences of ionizable residues in Gly-X-Y triplets of the collagen triple-helix. J. Biol. Chem., 1997, 272(50), 31441-31446.
Leikina, E.; Mertts, M.V.; Kuznetsova, N.; Leikin, S. Type I collagen is thermally unstable at body temperature. Proc. Natl. Acad. Sci. USA, 2002, 99(3), 1314-1318.
Han, R.; Zwiefka, A.; Caswell, C.C.; Xu, Y.; Keene, D.R.; Lukomska, E.; Zhao, Z.; Höök, M.; Lukomski, S. Assessment of prokaryotic collagen-like sequences derived from streptococcal Scl1 and Scl2 proteins as a source of recombinant GXY polymers. Appl. Microbiol. Biotechnol., 2006, 72(1), 109-115.
Xu, C.; Yu, Z.; Inouye, M.; Brodsky, B.; Mirochnitchenko, O. Expanding the family of collagen proteins: recombinant bacterial collagens of varying composition form triple-helices of similar stability. Biomacromolecules, 2010, 11(2), 348-356.
Han, R.; Caswell, C.C.; Lukomska, E.; Keene, D.R.; Pawlowski, M.; Bujnicki, J.M.; Kim, J.K.; Lukomski, S. Binding of the low-density lipoprotein by streptococcal collagen-like protein Scl1 of Streptococcus pyogenes. Mol. Microbiol., 2006, 61(2), 351-367.
Squeglia, F.; Bachert, B.; Romano, M.; Lukomski, S.; Berisio, R. Crystallization and preliminary X-ray crystallographic analysis of the variable domain of Scl2.3, a streptococcal collagen-like protein from invasive M3-type Streptococcus pyogenes. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 2013, 69(Pt 9), 1023-1025.
Squeglia, F.; Bachert, B.; De Simone, A.; Lukomski, S.; Berisio, R. The crystal structure of the streptococcal collagen-like protein 2 globular domain from invasive M3-type group A Streptococcus shows significant similarity to immunomodulatory HIV protein gp41. J. Biol. Chem., 2014, 289(8), 5122-5133.
Yu, Z.; Mirochnitchenko, O.; Xu, C.; Yoshizumi, A.; Brodsky, B.; Inouye, M. Noncollagenous region of the streptococcal collagen-like protein is a trimerization domain that supports refolding of adjacent homologous and heterologous collagenous domains. Protein Sci., 2010, 19(4), 775-785.
Humtsoe, J.O.; Kim, J.K.; Xu, Y.; Keene, D.R.; Höök, M.; Lukomski, S.; Wary, K.K. A streptococcal collagen-like protein interacts with the α2β1 integrin and induces intracellular signaling. J. Biol. Chem., 2005, 280(14), 13848-13857.
Caswell, C.C.; Lukomska, E.; Seo, N.S.; Höök, M.; Lukomski, S. Scl1-dependent internalization of group A Streptococcus via direct interactions with the α2β1 integrin enhances pathogen survival and re-emergence. Mol. Microbiol., 2007, 64(5), 1319-1331.
Caswell, C.C.; Barczyk, M.; Keene, D.R.; Lukomska, E.; Gullberg, D.E.; Lukomski, S. Identification of the first prokaryotic collagen sequence motif that mediates binding to human collagen receptors, integrins α2β1 and α11β1. J. Biol. Chem., 2008, 283(52), 36168-36175.
McNitt, D.H.; Choi, S.J.; Keene, D.R.; Van De Water, L.; Squeglia, F.; Berisio, R.; Lukomski, S. Surface-exposed loops and an acidic patch in the Scl1 protein of group A Streptococcus enable Scl1 binding to wound-associated fibronectin. J. Biol. Chem., 2018, 293(20), 7796-7810.
Caswell, C.C.; Han, R.; Hovis, K.M.; Ciborowski, P.; Keene, D.R.; Marconi, R.T.; Lukomski, S. The Scl1 protein of M6-type group A Streptococcus binds the human complement regulatory protein, factor H, and inhibits the alternative pathway of complement. Mol. Microbiol., 2008, 67(3), 584-596.
Reuter, M.; Caswell, C.C.; Lukomski, S.; Zipfel, P.F. Binding of the human complement regulators CFHR1 and factor H by streptococcal collagen-like protein 1 (Scl1) via their conserved C termini allows control of the complement cascade at multiple levels. J. Biol. Chem., 2010, 285(49), 38473-38485.
Gao, Y.; Liang, C.; Zhao, R.; Lukomski, S.; Han, R. The Scl1 of M41-type group A Streptococcus binds the high-density lipoprotein. FEMS Microbiol. Lett., 2010, 309(1), 55-61.
Påhlman, L.I.; Marx, P.F.; Mӧrgelin, M.; Lukomski, S.; Meijers, J.C.; Herwald, H. Thrombin-activatable fibrinolysis inhibitor binds to Streptococcus pyogenes by interacting with collagen-like proteins A and B. J. Biol. Chem., 2007, 282(34), 24873-24881.
Dohrmann, S.; Anik, S.; Olson, J.; Anderson, E.L.; Etesami, N.; No, H.; Snipper, J.; Nizet, V.; Okumura, C.Y. Role for streptococcal collagen-like protein 1 in M1T1 group A Streptococcus resistance to neutrophil extracellular traps. Infect. Immun., 2014, 82(10), 4011-4020.
Van De Water, L.; Varney, S.; Tomasek, J.J. Mechanoregulation of the myofibroblast in wound contraction, scarring, and fibrosis: opportunities for new therapeutic intervention. Adv. Wound Care (New Rochelle), 2013, 2(4), 122-141.
Gurtner, G.C.; Werner, S.; Barrandon, Y.; Longaker, M.T. Wound repair and regeneration. Nature, 2008, 453, 314-321.
Clark, R.A.; Lanigan, J.M.; DellaPelle, P.; Manseau, E.; Dvorak, H.F.; Colvin, R.B. Fibronectin and fibrin provide a provisional matrix for epidermal cell migration during wound reepithelialization. J. Invest. Dermatol., 1982, 79(5), 264-269.
Olczyk, P.; Mencner, Ł.; Komosinska-Vassev, K. The role of the extracellular matrix components in cutaneous wound healing. BioMed Res. Int., 2014, 2014747584
Xue, M.; Jackson, C.J. Extracellular matrix reorganization during wound healing and its impact on abnormal scarring. Adv. Wound Care, 2015, 4(3), 119-136.
Pankov, R.; Yamada, K.M. Fibronectin at a glance. J. Cell Sci., 2002, 115(Pt 20), 3861-3863.
Ffrench-Constant, C. Alternative splicing of fibronectin--many different proteins but few different functions. Exp. Cell Res., 1995, 221(2), 261-271.
Hynes, R.O. Fibronectins; Springer-Verlag: New York, NY, 1990.
To, W.S.; Midwood, K.S. Plasma and cellular fibronectin: distinct and independent functions during tissue repair. Fibrogenesis Tissue Repair, 2011, 4(1), 21.
Ffrench-Constant, C.; Hynes, R.O. Alternative splicing of fibronectin is temporally and spatially regulated in the chicken embryo. Development, 1989, 106(2), 375-388.
Ffrench-Constant, C.; Van De Water, L.; Dvorak, H.F.; Hynes, R.O. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J. Cell Biol., 1989, 109(2), 903-914.
Coito, A.J.; Brown, L.F.; Peters, J.H.; Kupiec-Weglinski, J.W.; Van De Water, L. Expression of fibronectin splicing variants in organ transplantation: A differential pattern between rat cardiac allografts and isografts. Am. J. Pathol., 1997, 150(5), 1757-1772.
Singh, P.; Reimer, C.L.; Peters, J.H.; Stepp, M.A.; Hynes, R.O.; Van De Water, L. The spatial and temporal expression patterns of integrin α9β1 and one of its ligands, the EIIIA segment of fibronectin, in cutaneous wound healing. J. Invest. Dermatol., 2004, 123(6), 1176-1181.
Muro, A.F.; Chauhan, A.K.; Gajovic, S.; Iaconcig, A.; Porro, F.; Stanta, G.; Baralle, F.E. Regulated splicing of the fibronectin EDA exon is essential for proper skin wound healing and normal lifespan. J. Cell Biol., 2003, 162(1), 149-160.
Longmate, W.M.; Lyons, S.P.; Chittur, S.V.; Pumiglia, K.M.; Van De Water, L.; DiPersio, C.M. Suppression of integrin α3β1 by α9β1 in the epidermis controls the paracrine resolution of wound angiogenesis. J. Cell Biol., 2017, 216(5), 1473-1488.
Leahy, D.J.; Aukhil, I.; Erickson, H.P. 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell, 1996, 84(1), 155-164.
Niimi, T.; Osawa, M.; Yamaji, N.; Yasunaga, K.; Sakashita, H.; Mase, T.; Tanaka, A.; Fujita, S. NMR structure of human fibronectin EDA. J. Biomol. NMR, 2001, 21(3), 281-284.
Liao, Y.F.; Gotwals, P.J.; Koteliansky, V.E.; Sheppard, D.; Van De Water, L. The EIIIA segment of fibronectin is a ligand for integrins α9β1 and α4β1 providing a novel mechanism for regulating cell adhesion by alternative splicing. J. Biol. Chem., 2002, 277(17), 14467-14474.
Shinde, A.V.; Bystroff, C.; Wang, C.; Vogelezang, M.G.; Vincent, P.A.; Hynes, R.O.; Van De Water, L. Identification of the peptide sequences within the EIIIA (EDA) segment of fibronectin that mediate integrin α9β1-dependent cellular activities. J. Biol. Chem., 2008, 283(5), 2858-2870.
Kohan, M.; Muro, A.F.; White, E.S.; Berkman, N. EDA-containing cellular fibronectin induces fibroblast differentiation through binding to α4β7 integrin receptor and MAPK/Erk 1/2-dependent signaling. FASEB J., 2010, 24(11), 4503-4512.
White, E.S.; Muro, A.F. Fibronectin splice variants: understanding their multiple roles in health and disease using engineered mouse models. IUBMB Life, 2011, 63(7), 538-546.
Singh, P.; Chen, C.; Pal-Ghosh, S.; Stepp, M.A.; Sheppard, D.; Van De Water, L. Loss of integrin α9β1 results in defects in proliferation, causing poor re-epithelialization during cutaneous wound healing. J. Invest. Dermatol., 2009, 129(1), 217-228.
Shinde, A.V.; Kelsh, R.; Peters, J.H.; Sekiguchi, K.; Van De Water, L.; McKeown-Longo, P.J. The α4β1 integrin and the EDA domain of fibronectin regulate a profibrotic pheotype in dermal fibroblasts. Matrix Biol., 2015, 41, 26-35.
Mitchell, K.; Szekeres, C.; Milano, V.; Svenson, K.B.; Nilsen-Hamilton, M.; Kreidberg, J.A.; DiPersio, C.M. α3β1 integrin in epidermis promotes wound angiogenesis and keratinocyte-to-endothelial-cell crosstalk through the induction of MRP3. J. Cell Sci., 2009, 122(Pt 11), 1778-1787.
Longmate, W.M.; Monichan, R.; Chu, M-L.; Tsuda, T.; Mahoney, M.G.; DiPersio, C.M. Reduced fibulin-2 contributes to loss of basement membrane integrity and skin blistering in mice lacking integrin α3β1 in the epidermis. J. Invest. Dermatol., 2014, 134(6), 1609-1617.
Julier, Z.; Martino, M.M.; de Titta, A.; Jeanbart, L.; Hubbell, J.A. The TLR4 agonist fibronectin extra domain A is cryptic, exposed by elastase-2; use in a fibrin matrix cancer vaccine. Sci. Rep., 2015, 5, 8569.
Okamura, Y.; Watari, M.; Jerud, E.S.; Young, D.W.; Ishizaka, S.T.; Rose, J.; Chow, J.C.; Strauss, J.F., III The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem., 2001, 276(13), 10229-10233.
Kelsh, R.; You, R.; Horzempa, C.; Zheng, M.; McKeown-Longo, P.J. Regulation of the innate immune response by fibronectin: Synergism between the III-1 and EDA domains. PLoS One, 2014, 9(7)e102974
Ozeri, V.; Rosenshine, I.; Mosher, D.F.; Fässler, R.; Hanski, E. Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol. Microbiol., 1998, 30, 625-637.
Joh, D.; Speziale, P.; Gurusiddappa, S.; Manor, J.; Höök, M. Multiple specificities of the staphylococcal and streptococcal fibronectin‐binding microbial surface components recognizing adhesive matrix molecules. Eur. J. Biochem., 1998, 258(2), 897-905.
Schwarz-Linek, U.; Werner, J.M.; Pickford, A.R.; Gurusiddappa, S.; Kim, J.H.; Pilka, E.S.; Briggs, J.A.; Gough, T.S.; Hӧӧk, M.; Campbell, I.D.; Potts, J.R. Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature, 2003, 423(6936), 177-181.
Yamaguchi, M.; Terao, Y.; Kawabata, S. Pleiotropic virulence factor - Streptococcus pyogenes fibronectin-binding proteins. Cell. Microbiol., 2013, 15(4), 503-511.
Hayes, C.S.; Williamson, H., Jr Management of group A beta-hemolytic streptococcal pharyngitis. Am. Fam. Physician, 2001, 63(8), 1557-1564.
Neeman, R.; Keller, N.; Barzilai, A.; Korenman, Z.; Sela, S. Prevalence of internalisation-associated gene, prtF1, among persisting group-A Streptococcus strains isolated from asymptomatic carriers. Lancet, 1998, 352(9145), 1974-1977.
Stjernquist-Desatnik, A.; Orrling, A.; Schalén, C.; Kamme, C. Penicillin tolerance in group A streptococci and treatment failure in streptococcal tonsillitis. Acta Otolaryngol., 1992, 492, 68-71.
Pichichero, M.E.; Casey, J.R.; Mayes, T.; Francis, A.B.; Marsocci, S.M.; Murphy, A.M.; Hoeger, W. Penicillin failure in streptococcal tonsillopharyngitis: causes and remedies. Pediatr. Infect. Dis. J., 2000, 19(9), 917-923.
Martin, J.M.; Green, M.; Barbadora, K.A.; Wald, E.R. Erythromycin-resistant group A streptococci in schoolchildren in Pittsburgh. N. Engl. J. Med., 2002, 346(16), 1200-1206.
Perez-Trallero, E.; Montes, M.; Orden, B.; Tamayo, E.; Garcia-Arenzana, J.; Marimon, J. Phenotypic and genotypic characterization of Streptococcus pyogenes displaying the MLSB-phenotype of macrolide resistance in Spain: 1999-2005. Antimicrob. Agents Chemother., 2007, 51(4), 1228-1233.
Lancefield, R.C. Persistence of type-specific antibodies in man following infection with group A streptococci. J. Exp. Med., 1959, 110(2), 271-292.
Cunningham, M.W. In: Gram-positive pathogens; Fischetti, V.A.; Novick, R.P.; Ferretti, J.J.; Portnoy, D.A.; Rood, J.I., Eds.; American Society for Microbiology Press: Washington, D.C., 2000; pp. 66-77.
Dale, J.B. Current status of group A streptococcal vaccine development. Adv. Exp. Med. Biol., 2008, 609, 53-63.
Steer, A.C.; Carapetis, J.R.; Dale, J.B.; Fraser, J.D.; Good, M.F.; Guilherme, L.; Moreland, N.J.; Mulholland, E.K.; Schodel, F.; Smeesters, P.R. Status of research and development of vaccines for Streptococcus pyogenes. Vaccine, 2016, 34(26), 2953-2958.
Steer, A.C.; Law, I.; Matatolu, L.; Beall, B.W.; Carapetis, J.R. Global emm type distribution of group A streptococci: systematic review and implications for vaccine development. Lancet Infect. Dis., 2009, 9(10), 611-616.
Guirguis, N.; Fraser, D.W.; Facklam, R.R.; El Kholy, A.; Wannamaker, L.W. Type-specific immunity and pharyngeal acquisition of group A Streptococcus. Am. J. Epidemiol., 1982, 116(6), 933-939.
Peng, Y.Y.; Yoshizumi, A.; Danon, S.J.; Glattauer, V.; Prokopenko, O.; Mirochnitchenko, O.; Yu, Z.; Inouye, M.; Werkmeister, J.A.; Brodsky, B.; Ramshaw, J.A. A Streptococcus pyogenes derived collagen-like protein as a non-cytotoxic and non-immunogenic cross-linkable biomaterial. Biomaterials, 2010, 31(10), 2755-2761.
Bhardwaj, G.; Mulligan, V.K.; Bahl, C.D.; Gilmore, J.M.; Harvey, P.J.; Cheneval, O.; Buchko, G.W.; Pulavarti, S.V.S.R.K.; Kaas, Q.; Eletsky, A.; Huang, P-S.; Johnsen, W.A.; Greisen, P., Jr; Rocklin, G.J.; Song, Y.; Linsky, T.W.; Watkins, A.; Rettie, S.A.; Xu, X.; Carter, L.P.; Bonneau, R.; Olson, J.M.; Coutsias, E.; Correnti, C.E.; Szyperski, T.; Craik, D.J.; Baker, D. Accurate de novo design of hyperstable constrained peptides. Nature, 2016, 538, 329.
Gaillard, V.; Galloux, M.; Garcin, D.; Eléouët, J-F.; Le Goffic, R.; Larcher, T.; Rameix-Welti, M-A.; Boukadiri, A.; Héritier, J.; Segura, J-M.; Baechler, E.; Arrell, M.; Mottet-Osman, G.; Nyanguile, O. A short double-stapled peptide inhibits respiratory syncytial virus entry and spreading. Antimicrob. Agents Chemother., 2017, 61(4), e02241-e16.
Wiedmann, M.M.; Tan, Y.S.; Wu, Y.; Aibara, S.; Xu, W.; Sore, H.F.; Verma, C.S.; Itzhaki, L.; Stewart, M.; Brenton, J.D.; Spring, D.R. Development of cell-permeable, non-helical constrained peptides to target a key protein–protein interaction in ovarian cancer. Angewandte Chemie International Edition, 2017, 56(2), 524-529.
Nizet, V.; Ohtake, T.; Lauth, X.; Trowbridge, J.; Rudisill, J.; Dorschner, R.A.; Pestonjamasp, V.; Piraino, J.; Huttner, K.; Gallo, R.L. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature, 2001, 414(6862), 454-457.
Dorschner, R.A.; Pestonjamasp, V.K.; Tamakuwala, S.; Ohtake, T.; Rudisill, J.; Nizet, V.; Agerberth, B.; Gudmundsson, G.H.; Gallo, R.L. Cutaneous injury induces the release of cathelicidin anti-microbial peptides active against group A Streptococcus. J. Invest. Dermatol., 2001, 117(1), 91-97.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Page: [1933 - 1945]
Pages: 13
DOI: 10.2174/0929867325666180831165704
Price: $58

Article Metrics

PDF: 22