Granadaene

Last updated
Granadaene
Granadaene.svg
Names
IUPAC name
(2S)-5-Amino-2-[[(2E,4E,6E,8E,10E,12E,14E,16E,18E,20E,22E,24E)-27-[(2R,3R,4R,5R,6S)-3,4,5-trihydroxy-6-methyloxan-2-yl]oxyoctacosa-2,4,6,8,10,12,14,16,18,20,22,24-dodecaenoyl]amino]pentanoic acid
Identifiers
3D model (JSmol)
ChemSpider
PubChem CID
  • InChI=1S/C39H52N2O8/c1-31(48-39-37(45)36(44)35(43)32(2)49-39)27-24-22-20-18-16-14-12-10-8-6-4-3-5-7-9-11-13-15-17-19-21-23-25-29-34(42)41-33(38(46)47)28-26-30-40/h3-25,29,31-33,35-37,39,43-45H,26-28,30,40H2,1-2H3,(H,41,42)(H,46,47)/b4-3+,7-5+,8-6+,11-9+,12-10+,15-13+,16-14+,19-17+,20-18+,23-21+,24-22+,29-25+/t31?,32-,33-,35-,36+,37+,39+/m0/s1
    Key: PPFISAQUKQQDHW-OBEWLBDZSA-N
  • C[C@H]1[C@H](O)[C@@H](O)[C@@H](O)[C@@H](O1)OC(C)C/C=C/C=C/C=C/C=C/C=C/C=C/C=C/C=C/C=C/C=C/C=C/C=C/C(=O)N[C@@H](CCCN)C(=O)O
Properties
C39H52N2O8
Molar mass 676.851 g·mol−1
Except where otherwise noted, data are given for materials in their standard state (at 25 °C [77 °F], 100 kPa).

Granadaene is the trivial name of a polyene of non-isoprenoid biosynthetic origin, that constitutes the red pigment characteristic of Streptococcus agalactiae (group B streptococcus).

Contents

Characteristics

Granadaene contains a conjugated system made up of a linear chain of 12 conjugated carbon-carbon double bonds which is connected to the amino acid ornithine at one end and the sugar rhamnose at the other. [1] [2] Granadaene contains 12 conjugated double bonds, a feature which is unprecedented among non-isoprenoid pigments.

Granadaene is dark red, odorless, insoluble in water, methanol, ethanol, diethyl ether, acetone, hexane, dimethyl sulfoxide (DMSO), acetonitrile, tetrahydrofuran, chloroform, and in most solvents, it is soluble in DMSO–0.1% trifluoroacetic acid (TFA). [1] Granadaene, can be extracted from cultures of S.agalactiae in granada broth (granada medium without agar) with 0.1 M potassium hydroxide (KOH) and purified by size-exclusion chromatography on Sephadex LH using DMSO–0.1%TFA. [1]

Streptococcus agalactiae in granada broth Streptococcus agalactiae in granada broth.JPG
Streptococcus agalactiae in granada broth
Streptococcus agalactiae on granada agar, anaerobic incubation Streptococcus agalactiae on Granada medium.jpg
Streptococcus agalactiae on granada agar, anaerobic incubation
Ultraviolet/visible spectrum of granadaene, in DMSO+TFA Granadaene UV-VIS spectrum DMSO-TFA.jpg
Ultraviolet/visible spectrum of granadaene, in DMSO+TFA
Proposed metabolic pathway for granadaene biosynthesis Granadaene pathway.jpg
Proposed metabolic pathway for granadaene biosynthesis

The fine-structure of the ultraviolet-visible absorption spectrum of the granadaene (in DMSO/TFA) is almost identical to that of a carotene with a similar conjugated system of 12 double bonds (e.g. alpha-carotene), which is why the GBS pigment was considered to be a carotene for many years. [3]

Non-terpenoid polyenes up to 10 conjugated double bonds are also a bizarre class of biologically natural products (laetiporic acids) found in the basidiomycete Laetiporus sulphureus. [4]

Granadaene and S.agalactiae detection and identification

Production of the red pigment granadaene is a phenotypic trait specific to β-hemolytic GBS, and because of that, detection of red colonies from clinical samples, when cultivated on granada medium, allows the straightforward identification of GBS. [5] [6] [7]

Biological relevance

Granadaene is an organic compound produced by S.agalactiae. It is the product of a metabolic pathway similar to that of biosynthesis of fatty acids. The enzymes necessary for the biosynthesis of granadaene in GBS are coded by a gene cluster of 12 genes, the cyl operon, Among the cyl operon, the cylE gene is required for pigment production, and transcription of cyl genes is regulated by the CovR/S two-component system, [8] and a pathway for the pigment biosynthesis requiring all the genes of the cyl operon has been proposed.

Like the biosynthesis of the pigment, the hemolytic activity also requires in GBS the 12 genes of the cyl operon. [9] [10] Moreover,it has been proposed that granadaene is indeed the hemolysin of S.agalactiae

The pigment is localized, in GBS, in the cell membrane, [3] where it could play a role in membrane stabilization, similar to the role of carotenes in other bacterial membranes. [11] In addition to S.agalactiae the presence of granadaene and the cyl genes has been reported in pigmented Acidipropionibacterium spp. (former Propionibacterium) as A.jensenii, A.thoenii, and A.virtanenii [12] , where it can cause defects such as red spots in some cheeses. [13] Probably granadaene is also present in other related species such as Pseudopropionibacterium rubrum. [8] [13] [14] Granadaene is also produced by strains of Lactocococcus garvieae/petaury/formosensis group where the cyl cluster is also present. [15]

The cyl genes have been cloned in Lactococcus lactis (a non-hemolytic non-pigmented Gram-positive bacterium) and the expression of the GBS cyl operon conferred hemolysis, pigmentation, and cytotoxicity to Lactococcus lactis. Proving that the expression of the genes of the cyl operon is sufficient for Granadaene production in a heterologous host. [16]

Granadaene and GBS Virulence

The hemolytic activity of granadene is strongly linked to the length of its polyene chain. [17] [18]

It has been proposed that granadaene is indeed the hemolysin of S.agalactiae, the GBS hemolysin is a broad-spectrum cytolysin able to destroy many eukaryotic cells, including platelets. Because of this, granadaene is considered an important virulence factor for GBS. [8] [19] [20] [21] [22] [23] [24] [25]

Nevertheless, 1–5% of GBS strains are non-hemolytic and do not produce pigment. [8] These non-hemolytic and non-pigmented GBS strains (lacking pigment and hemolysin) are considered less virulent because of that. [19] [21] [26] [27]

Related Research Articles

<i>Streptococcus</i> Genus of bacteria

Streptococcus is a genus of gram-positive or spherical bacteria that belongs to the family Streptococcaceae, within the order Lactobacillales, in the phylum Bacillota. Cell division in streptococci occurs along a single axis, thus when growing they tend to form pairs or chains, which may appear bent or twisted. This differs from staphylococci, which divide along multiple axes, thereby generating irregular, grape-like clusters of cells. Most streptococci are oxidase-negative and catalase-negative, and many are facultative anaerobes.

<span class="mw-page-title-main">Group A streptococcal infection</span> Medical condition

Group A streptococcal infections are a number of infections with Streptococcus pyogenes, a group A streptococcus (GAS). S. pyogenes is a species of beta-hemolytic Gram-positive bacteria that is responsible for a wide range of infections that are mostly common and fairly mild. If the bacteria enters the bloodstream, the infection can become severe and life-threatening, and is called an invasive GAS (iGAS).

<i>Streptococcus pyogenes</i> Species of bacterium

Streptococcus pyogenes is a species of Gram-positive, aerotolerant bacteria in the genus Streptococcus. These bacteria are extracellular, and made up of non-motile and non-sporing cocci that tend to link in chains. They are clinically important for humans, as they are an infrequent, but usually pathogenic, part of the skin microbiota that can cause group A streptococcal infection. S. pyogenes is the predominant species harboring the Lancefield group A antigen, and is often called group A Streptococcus (GAS). However, both Streptococcus dysgalactiae and the Streptococcus anginosus group can possess group A antigen as well. Group A streptococci, when grown on blood agar, typically produce small (2–3 mm) zones of beta-hemolysis, a complete destruction of red blood cells. The name group A (beta-hemolytic) Streptococcus is thus also used.

<span class="mw-page-title-main">Streptococcal pharyngitis</span> Medical condition

Streptococcal pharyngitis, also known as streptococcal sore throat, is pharyngitis caused by Streptococcus pyogenes, a gram-positive, group A streptococcus. Common symptoms include fever, sore throat, red tonsils, and enlarged lymph nodes in the front of the neck. A headache and nausea or vomiting may also occur. Some develop a sandpaper-like rash which is known as scarlet fever. Symptoms typically begin one to three days after exposure and last seven to ten days.

<i>Streptococcus agalactiae</i> Species of bacterium

Streptococcus agalactiae is a gram-positive coccus with a tendency to form chains. It is a beta-hemolytic, catalase-negative, and facultative anaerobe.

<span class="mw-page-title-main">Group B streptococcal infection</span> Medical condition

Group B streptococcal infection, also known as Group B streptococcal disease or just Group B strep infection, is the infectious disease caused by the bacterium Streptococcus agalactiae. Streptococcus agalactiae is the most common human pathogen belonging to group B of the Lancefield classification of streptococci—hence the name of group B stretococcal (GBS). Infection with GBS can cause serious illness and sometimes death, especially in newborns, the elderly, and people with compromised immune systems. The most severe form of group B streptococcal disease is neonatal meningitis in infants, which is frequently lethal and can cause permanent neuro-cognitive impairment.

<i>Streptococcus sanguinis</i> Species of bacterium

Streptococcus sanguinis, formerly known as Streptococcus sanguis, is a Gram-positive facultative anaerobic coccus species of bacteria and a member of the Viridans Streptococcus group. S. sanguinis is a normal inhabitant of the healthy human mouth where it is particularly found in dental plaque, where it modifies the environment to make it less hospitable for other strains of Streptococcus that cause cavities, such as Streptococcus mutans.

<span class="mw-page-title-main">Clobetasone</span> Chemical compound

Clobetasone (INN) is a corticosteroid used in dermatology, for treating such skin inflammation as seen in eczema, psoriasis and other forms of dermatitis, and ophthalmology. Topical clobetasone butyrate has shown minimal suppression of the hypothalamic–pituitary–adrenal axis.

<i>Arcanobacterium haemolyticum</i> Species of bacterium

Arcanobacterium haemolyticum is a species of bacteria classified as a gram-positive bacillus. It is catalase-negative, facultative anaerobic, beta-hemolytic, and not motile. It has been known to cause head and neck infections, pharyngitis, and sinusitis.

Streptolysins are two homogenous exotoxins from Streptococcus pyogenes. Types include streptolysin O, which is oxygen-labile, and streptolysin S, which is oxygen-stable.

<span class="mw-page-title-main">CAMP test</span> Microbiological method for identification

The CAMP test (Christie–Atkins–Munch-Petersen) is a test to identify group B β-hemolytic streptococci based on their formation of a substance, CAMP factor, that enlarges the area of hemolysis formed by the β-hemolysin elaborated from Staphylococcus aureus.

<i>Streptococcus canis</i> Species of bacterium

Streptococcus canis is a group G beta-hemolytic species of Streptococcus. It was first isolated in dogs, giving the bacterium its name. These bacteria are characteristically different from Streptococcus dysgalactiae, which is a human-specific group G species that has a different phenotypic chemical composition. S. canis is important to the skin and mucosal health of cats and dogs, but under certain circumstances, these bacteria can cause opportunistic infections. These infections were known to afflict dogs and cats prior to the formal description of the species in Devriese et al., 1986. However, additional studies revealed cases of infection in other mammal species, including cattle and even humans. Instances of mortality from S. canis in humans are very low with only a few reported cases, while actual instances of infection may be underreported due to mischaracterizations of the bacteria as S. dysgalactiae. This species, in general, is highly susceptible to antibiotics, and plans to develop a vaccine to prevent human infections are currently being considered.

<i>Streptococcus dysgalactiae</i> Species of bacterium

Streptococcus dysgalactiae is a gram positive, beta-haemolytic, coccal bacterium belonging to the family Streptococcaceae. It is capable of infecting both humans and animals, but is most frequently encountered as a commensal of the alimentary tract, genital tract, or less commonly, as a part of the skin flora. The clinical manifestations in human disease range from superficial skin-infections and tonsillitis, to severe necrotising fasciitis and bacteraemia. The incidence of invasive disease has been reported to be rising. Several different animal species are susceptible to infection by S. dysgalactiae, but bovine mastitis and infectious arthritis in lambs have been most frequently reported.

<i>Streptococcus iniae</i> Species of bacterium

Streptococcus iniae is a species of Gram-positive, sphere-shaped bacterium belonging to the genus Streptococcus. Since its isolation from an Amazon freshwater dolphin in the 1970s, S. iniae has emerged as a leading fish pathogen in aquaculture operations worldwide, resulting in over US$100M in annual losses. Since its discovery, S. iniae infections have been reported in at least 27 species of cultured or wild fish from around the world. Freshwater and saltwater fish including tilapia, red drum, hybrid striped bass, and rainbow trout are among those susceptible to infection by S. iniae. Infections in fish manifest as meningoencephalitis, skin lesions, and septicemia.

Perianal cellulitis, also known as perianitis or perianal streptococcal dermatitis, is a bacterial infection affecting the lower layers of the skin (cellulitis) around the anus. It presents as bright redness in the skin and can be accompanied by pain, difficulty defecating, itching, and bleeding. This disease is considered a complicated skin and soft tissue infection (cSSTI) because of the involvement of the deeper soft tissues.

Bacteriophage T12 is a bacteriophage that infects Streptococcus pyogenes bacteria. It is a proposed species of the family Siphoviridae in the order Caudovirales also known as tailed viruses. It converts a harmless strain of bacteria into a virulent strain. It carries the speA gene which codes for erythrogenic toxin A. speA is also known as streptococcal pyogenic exotoxin A, scarlet fever toxin A, or even scarlatinal toxin. Note that the name of the gene "speA" is italicized; the name of the toxin "speA" is not italicized. Erythrogenic toxin A converts a harmless, non-virulent strain of Streptococcus pyogenes to a virulent strain through lysogeny, a life cycle which is characterized by the ability of the genome to become a part of the host cell and be stably maintained there for generations. Phages with a lysogenic life cycle are also called temperate phages. Bacteriophage T12, proposed member of family Siphoviridae including related speA-carrying bacteriophages, is also a prototypic phage for all the speA-carrying phages of Streptococcus pyogenes, meaning that its genome is the prototype for the genomes of all such phages of S. pyogenes. It is the main suspect as the cause of scarlet fever, an infectious disease that affects small children.

In molecular biology, the FasX small RNA (fibronectin/fibrinogen-binding/haemolytic-activity/streptokinase-regulator-X) is a non-coding small RNA (sRNA) produced by all group A Streptococcus. FasX has also been found in species of group D and group G Streptococcus. FasX regulates expression of secreted virulence factor streptokinase (SKA), encoded by the ska gene. FasX base pairs to the 5' end of the ska mRNA, increasing the stability of the mRNA, resulting in elevated levels of streptokinase expression. FasX negatively regulates the expression of pili and fibronectin-binding proteins on the bacterial cell surface. It binds to the 5' untranslated region of genes in the FCT-region in a serotype-specific manner, reducing the stability of and inhibiting translation of the pilus biosynthesis operon mRNA by occluding the ribosome-binding site through a simple Watson-Crick base-pairing mechanism.

<span class="mw-page-title-main">Lancefield grouping</span> System for classifying streptococci bacteria

Lancefield grouping is a system of classification that classifies catalase-negative Gram-positive cocci based on the carbohydrate composition of bacterial antigens found on their cell walls. The system, created by Rebecca Lancefield, was historically used to organize the various members of the family Streptococcaceae, which includes the genera Lactococcus and Streptococcus, but now is largely superfluous due to explosive growth in the number of streptococcal species identified since the 1970s. However, it has retained some clinical usefulness even after the taxonomic changes, and as of 2018, Lancefield designations are still often used to communicate medical microbiological test results.

<span class="mw-page-title-main">Granada medium</span>

Granada medium is a selective and differential culture medium designed to selectively isolate Streptococcus agalactiae and differentiate it from other microorganisms. Granada Medium was developed by Manuel Rosa-Fraile et al. at the Service of Microbiology in the Hospital Virgen de las Nieves in Granada (Spain).

Streptococcosis is an infectious disease caused by bacteria of the genus Steptococcus. This disease is most common among horses, guinea pigs, dogs, cats, and fish with symptoms varying based on the streptococcal species involved. In humans, this disease typically involves a throat infection and is called streptococcal pharyngitis or strep throat.

References

  1. 1 2 3 Rosa-Fraile M, Rodríguez-Granger J, Haidour-Benamin A, Cuerva JM, Sampedro A (2006). "Granadaene: Proposed Structure of the Group B Streptococcus Polyenic Pigment". Appl Environ Microbiol. 72 (9): 6367–6370. Bibcode:2006ApEnM..72.6367R. doi:10.1128/aem.00756-06. PMC   1563658 . PMID   16957264.
  2. ↑ Paradas M, Jurado R, Haidour A, Rodríguez Granger J, Sampedro Martínez A, de la Rosa Fraile M, Robles R, Justicia J, Cuerva JM (2012). "Clarifying the structure of granadaene: Total synthesis of related analogue - granadaene and confirmation of its absolute stereochemistry". Bioorg Med Chem. 20 (22): 6655–6661. doi:10.1016/j.bmc.2012.09.017. PMID   23043725.
  3. 1 2 Merrit K, Jacobs NJ (1978). "Characterization and Incidence of Pigment Production by Human Clinical Group B Streptococci". J Clin Microbiol. 8 (1): 105–107. doi:10.1128/jcm.8.1.105-107.1978. PMC   275130 . PMID   353069.
  4. ↑ Seibold PS. Lenz C. Gressler M. Hoffmeister D. (2020). "The Laetiporus polyketide synthase LpaA produces a series of antifungal polyenes". J Antibiot (Tokyo). 73 (10): 711–720. doi:10.1038/s41429-020-00362-6. PMC   7473843 . PMID   32820242.
  5. ↑ M Rosa-Fraile, J Rodriguez-Granger, M Cueto-Lopez, A Sampedro, E B Gaye, J M Haro, A Andreu (1999). "Use of Granada medium to detect group B streptococcal colonization in pregnant women". J Clin Microbiol. 37 (8): 2674–2677. doi:10.1128/JCM.37.8.2674-2677.1999. PMC   85311 . PMID   10405420.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  6. ↑ Verani JR, McGee L, Schrag SJ (2010). "Prevention of perinatal group B streptococcal disease: revised guidelines from CDC, 2010" (PDF). MMWR Recomm Rep. 59(RR-10): 1–32.
  7. ↑ Filkins L , Hauser J, Robinson-Dunn B, Tibbetts R, Boyanton B , Revell P. "Guidelines for the Detection and Identification of Group B Streptococcus. 2021". American Society for Microbiology. Retrieved 23 May 2023.{{cite web}}: CS1 maint: multiple names: authors list (link)
  8. 1 2 3 4 Rosa-Fraile M, Dramsi S, Spellerberg B (2014). "Group B streptococcal haemolysin and pigment, a tale of twins". FEMS Microbiol. Rev. 38 (5): 932–946. doi:10.1111/1574-6976.12071. PMC   4315905 . PMID   24617549.
  9. ↑ Spellerberg B, Pohl B, Haase G, Martin S, Weber-Heynemann J, Lütticken R (1999). "Identification of genetic determinants for the hemolytic activity of Streptococcus agalactiae by ISS1 transposition". J. Bacteriol. 181 (10): 3212–3219. doi:10.1128/JB.181.10.3212-3219.1999. PMC   93778 . PMID   10322024.
  10. ↑ Spellerberg B, Martin S, Brandt C, Lütticken R (2000). "The cyl genes of Streptococcus agalactiae are involved in the production of pigment". FEMS Microbiol. Lett. 188 (2): 125–128. doi: 10.1111/j.1574-6968.2000.tb09182.x . PMID   10913694.
  11. ↑ Taylor RF (1984). "Bacterial tryterpenoids". Microbiol. Rev. 48 (3): 181–198. doi:10.1128/MMBR.48.3.181-198.1984. PMC   373008 . PMID   6387426.
  12. ↑ Deptula P, Loivamaa L , Smolander OP, Laine P , Roberts RJ, Piironen V, Paulin L, Savijoki K, Auvinen P, Varmanen P (2019). "Red-Brown Pigmentation of Acidipropionibacterium jensenii Is Tied to Haemolytic Activity and cyl-Like Gene Cluster". Microorganisms 7: 512. https://doi.org/10.3390/microorganisms7110512 |https://pmc.ncbi.nlm.nih.gov/articles/PMC6920887/%7C
  13. 1 2 Vanberg C, Lutnaes BF, Langsrud T, Nees IF, Holo H (2007). "Propionibacterium jensenii produces the polyene pigment granadaene and has hemolytic properties similar to those of Streptococcus agalactiae". Appl Environ Microbiol. 73 (17): 5501–5506. Bibcode:2007ApEnM..73.5501V. doi:10.1128/AEM.00545-07. PMC   2042088 . PMID   17630313.
  14. ↑ Masanori Saito, Noriko Shinozaki-Kuwahara, Osamu Tsudukibashi, Tomomi Hashizume-Takizawa, Ryoki Kobayashi, Tomoko Kurita-Ochiai (2018). "Pseudopropionibacterium rubrum sp. nov., a novel red-pigmented species isolated from human gingival sulcus". Microbiol Immunol. 62 (6): 388–394. doi: 10.1111/1348-0421.12592 . PMID   29687917. S2CID   22322865.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  15. ↑ Neuzil-Bunesova V, Ramirez Garcia A, Modrackova N, Makovska M, Sabolova M, Spröer C, Bunk B, Blom J, Schwab C (2022). "Feed Insects as a Reservoir of Granadaene-Producing Lactococci". Front. Microbiol. 13: Art 848490. doi: 10.3389/fmicb.2022.848490 . PMC   9125021 . PMID   35615513.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  16. ↑ Armistead B, Whidbey C, Iyer LM, Herrero-Foncubierta P, Quach P, Haidour A, Aravind L, Cuerva JM, Jaspan HB, Rajagopal L. (2020). "The cyl Genes Reveal the Biosynthetic and Evolutionary Origins of the Group B Streptococcus Hemolytic Lipid, Granadaene". Front. Microbiol. 10: 3123. doi: 10.3389/fmicb.2019.03123 . PMC   6985545 . PMID   32038561.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  17. ↑ Kristanc L, Božič B, Jokhadar ŠZ, Dolenc MS, Gomišček G. (2019). "The pore-forming action of polyenes: From model membranes to living organisms". Biochim Biophys Acta Biomembr. 186 (2): 418–430. doi: 10.1016/j.bbamem.2018.11.006 . PMID   30458121. S2CID   53735664.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  18. ↑ Armistead B, Herrero-Foncubierta P, Coleman M, Quach P, Whidbey C, Justicia J, Tapia R, Casares R, Millán A, Haidour A, Rodriguez Granger J, Vornhagen J, Santana-Ufret V, Merillat S, Waldorf KA, Cuerva JM, Rajagopal L (2020). "Lipid analogs reveal features critical for hemolysis and diminish granadaene mediated Group B Streptococcus infection". Nature Communications. 11 (1): 1502. Bibcode:2020NatCo..11.1502A. doi:10.1038/s41467-020-15282-0. PMC   7083881 . PMID   32198389 . Retrieved 30 May 2022.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  19. 1 2 Whidbey C, Harrell MI, Burnside K, Ngo L, Becraft AK, Iyer LM, Aravind L, Hitti J, Waldorf KM, Rajagopal L (2013). "A hemolytic pigment of Group B Streptococcus allows bacterial penetration of human placenta" (PDF). J Exp Med. 210 (6): 1265–1281. doi:10.1084/jem.20122753. PMC   3674703 . PMID   23712433.
  20. ↑ Liu Y, Liu J. (2022). "Group B Streptococcus: Virulence Factors and Pathogenic Mechanism". Microorganisms. 15 (12): 2483. doi: 10.3390/microorganisms10122483 . PMC   9784991 . PMID   36557736.
  21. 1 2 Whidbey C, Vornhagen J, Gendrin C, Boldenow E, Samson JM, Doering K, Ngo L, Ezekwe EA Jr, Gundlach JH, Elovitz MA, Liggitt D, Duncan JA, Adams Waldorf KM, Rajagopal L (2015). "A streptococcal lipid toxin induces membrane permeabilization and pyroptosis leading to fetal injury". EMBO Mol. Med. 7 (4): 488–505. doi:10.15252/emmm.201404883. PMC   4403049 . PMID   25750210.
  22. ↑ Armistead B, Oler E, Adams Waldorf K, Rajagopal L. (2019). "The Double Life of Group B Streptococcus: Asymptomatic Colonizer and Potent Pathogen". J Mol Biol. 431 (16): 2914–2931. doi:10.1016/j.jmb.2019.01.035. PMC   6646060 . PMID   30711542.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  23. ↑ Armistead B, Herrero-Foncubierta P, Coleman M, Quach P, Whidbey C, Justicia J, Tapia R, Casares R, Millán A, Haidour A, Granger JR, Vornhagen J, Santana-Ufret V, Merillat S, Adams Waldorf K, Cuerva JM, Rajagopal L. (2020). "Lipid analogs reveal features critical for hemolysis and diminish granadaene mediated Group B Streptococcus infection". Nat. Commun. 11 (1): 1502. Bibcode:2020NatCo..11.1502A. doi:10.1038/s41467-020-15282-0. PMC   7083881 . PMID   32198389.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  24. ↑ Huebner EM, Gudjónsdóttir MJ, Dacanay MB, Nguyen S, Brokaw A, Sharma K, Elfvin A, Hentz E, Rivera YR, Burd N, Shivakumar M, Coler B, Li M, Li A, Munson J, Orvis A, Coleman M, Jacobsson B, Rajagopal L, Adams Waldorf KM. (2022). "Virulence, phenotype and genotype characteristics of invasive group B Streptococcus isolates obtained from Swedish pregnant women and neonates". Ann Clin Microbiol Antimicrob. 21 (1): 43. doi: 10.1186/s12941-022-00534-2 . PMC   9560721 . PMID   36229877.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  25. ↑ Jahn, K.; Shumba, P.; Quach, P.; Müsken, M.; Wesche, J.; Greinacher, A.; Rajagopal, L.; Hammerschmidt, S.; Siemens, N. (2022). "Group B Streptococcal Hemolytic Pigment Impairs Platelet Function in a Two-Step Process". Cells. 11 (10): 1637. doi: 10.3390/cells11101637 . PMC   9139542 . PMID   35626674.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  26. ↑ Rodriguez-Granger J, Spellerberg B, Asam D, Rosa-Fraile M (2015). "Non-haemolytic and non-pigmented group b streptococcus, an infrequent cause of early onset neonatal sepsis". Pathogens and Disease. 73 (9): ftv089. doi:10.1093/femspd/ftv089. PMC   4626576 . PMID   26449711.
  27. ↑ Armistead B, Quach P, Snyder JM, Santana-Ufret V, Furuta A, Brokaw A, Rajagopal L. (2020). "Hemolytic membrane vesicles of Group B Streptococcus promote infection". The Journal of Infectious Diseases. jiaa548 (8): 1488–1496. doi:10.1093/infdis/jiaa548. PMC   8064051 . PMID   32861213.{{cite journal}}: CS1 maint: multiple names: authors list (link)
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