Bacterial hyaluronidase promotes ascending GBS infection and preterm birth

mBio

Volumn 7, Issue 3, 2016, Pages

  Vornhagen, Jay ^a,b   Quach, Phoenicia ^b   Boldenow, Erica ^b   Merillat, Sean ^b   Whidbey, Christopher ^a,b   Ngo, Lisa Y ^b   Adams Waldorf, K M ^c   Rajagopal, Lakshmi ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIDASE; HYALURONOGLUCOSAMINIDASE; VIRULENCE FACTOR;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; FEMALE; FETUS; FETUS DEATH; GROUP B STREPTOCOCCAL INFECTION; HUMAN; HUMAN CELL; IMMUNE EVASION; IMMUNE RESPONSE; MOUSE; NONHUMAN; PREMATURE LABOR; PRIORITY JOURNAL; UTERINE CERVICITIS; VAGINA SMEAR; AMNION FLUID; BLOOD; COMPLICATION; ENZYMOLOGY; GENITAL TRACT INFECTION; IMMUNOLOGY; INFLAMMATION; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; NEWBORN; PLACENTA; PREGNANCY; PREGNANCY COMPLICATION; PREMATURITY; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS INFECTION; UTERUS; VAGINA;

AMNIOTIC FLUID; FEMALE; HUMANS; HYALURONOGLUCOSAMINIDASE; INFANT, NEWBORN; INFLAMMATION; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PREMATURE BIRTH; REPRODUCTIVE TRACT INFECTIONS; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS AGALACTIAE; UTERUS; VAGINA; VIRULENCE FACTORS;

EID: 84979047236     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00781-16     Document Type: Article

References (46)

1. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE, Child Health Epidemiology Reference Group of WHO, UNICEF. 2012. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 379: 2151-2161. http:// dx.doi.org/10.1016/S0140-6736(12)60560-1.
2. Romero R, Dey SK, Fisher SJ. 2014. Preterm labor: one syndrome, many causes. Science 345: 760-765. http://dx.doi.org/10.1126/science.1251816.
3. Katz J, Lee AC, Kozuki N, Lawn JE, Cousens S, Blencowe H, Ezzati M, Bhutta ZA, Marchant T, Willey BA, Adair L, Barros F, Baqui AH, Christian P, Fawzi W, Gonzalez R, Humphrey J, Huybregts L, Kolsteren P, Mongkolchati A, Mullany LC, Ndyomugyenyi R, Nien JK, Osrin D, Roberfroid D, Sania A, Schmiegelow C, Silveira MF, Tielsch J, Vaidya A, Velaphi SC, Victora CG, Watson-Jones D, Black RE. 2013. Mortality risk in preterm and small-for-gestational-age infants in lowincome and middle-income countries: a pooled country analysis. Lancet 382: 417-425. http://dx.doi.org/10.1016/S0140-6736(13)60993-9.
4. Lawn JE, Gravett MG, Nunes TM, Rubens CE, Stanton C, GAPPS Review Group. 2010. Global report on preterm birth and stillbirth (1 of 7): definitions, description of the burden and opportunities to improve data. BMC Pregnancy Childbirth 10(Suppl 1): S1. http://dx.doi.org/10.1186/1471-2393-10-S1-S1.
5. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, Adler A, Vera Garcia C, Rohde S, Say L, Lawn JE. 2012. National, regional, and worldwide estimates of preterm birthrates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379: 2162-2172. http://dx.doi.org/10.1016/ S0140-6736(12)60820-4.
6. Rubens CE, Gravett MG, Victora CG, Nunes TM, GAPPS Review Group. 2010. Global report on preterm birth and stillbirth (7 of 7): mobilizing resources to accelerate innovative solutions (global action agenda). BMC Pregnancy Childbirth 10(Suppl 1): S7. http://dx.doi.org/10.1186/1471-2393-10-S1-S7.
7. Slattery MM, Morrison JJ. 2002. Preterm delivery. Lancet 360: 1489-1497. http://dx.doi.org/10.1016/S0140-6736(02)11476-0.
8. Blencowe H, Cousens S, Chou D, Oestergaard M, Say L, Moller AB, Kinney M, Lawn J, Born Too Soon Preterm Birth Action Group. 2013. Born too soon: the global epidemiology of 15 million preterm births. Reprod Health 10(Suppl 1): S2. http://dx.doi.org/10.1186/1742-4755-10-S1-S2.
9. Patel RM, Kandefer S, Walsh MC, Bell EF, Carlo WA, Laptook AR, Sánchez PJ, Shankaran S, Van Meurs KP, Ball MB, Hale EC, Newman NS, Das A, Higgins RD, Stoll BJ, Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. 2015. Causes and timing of death in extremely premature infants from 2000 through 2011. N Engl J Med 372: 331-340. http:// dx.doi.org/10.1056/NEJMoa1403489.
10. Nold C, Anton L, Brown A, Elovitz M. 2012. Inflammation promotes a cytokine response and disrupts the cervical epithelial barrier: a possible mechanism of premature cervical remodeling and preterm birth. Am J Obstet Gynecol 206: 208.e1-208e7. http://dx.doi.org/10.1016/ j.ajog.2011.12.036.
11. Romero R, Gonzalez R, Sepulveda W, Brandt F, Ramirez M, Sorokin Y, Mazor M, Treadwell MC, Cotton DB. 1992. Infection and labor. VIII. Microbial invasion of the amniotic cavity in patients with suspected cervical incompetence: prevalence and clinical significance. Am J Obstet Gynecol 167: 1086-1091. http://dx.doi.org/10.1016/S0002-9378(12)80043-3.
12. Hillier SL, Krohn MA, Kiviat NB, Watts DH, Eschenbach DA. 1991. Microbiologic causes and neonatal outcomes associated with chorioamnion infection. Am J Obstet Gynecol 165: 955-961. http://dx.doi.org/10.1016/0002-9378(91)90447-Y.
13. Ueno T, Niimi H, Yoneda N, Yoneda S, Mori M, Tabata H, Minami H, Saito S, Kitajima I. 2015. Eukaryote-made thermostable DNA polymerase enables rapid PCR-based detection of mycoplasma, ureaplasma and other bacteria in the amniotic fluid of preterm labor cases. PLoS One 10: e0129032. http://dx.doi.org/10.1371/journal.pone.0129032.
14. Goldenberg RL, Hauth JC, Andrews WW. 2000. Intrauterine infection and preterm delivery. N Engl J Med 342: 1500-1507. http://dx.doi.org/10.1056/NEJM200005183422007.
15. 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. J Exp Med 210: 1265-1281. http://dx.doi.org/10.1084/jem.20122753.
16. Bastek JA, Gómez LM, Elovitz MA. 2011. The role of inflammation and infection in preterm birth. Clin Perinatol 38: 385-406. http://dx.doi.org/10.1016/j.clp.2011.06.003.
17. Hillier SL, Martius J, Krohn M, Kiviat N, Holmes KK, Eschenbach DA. 1988. A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med 319: 972-978. http:// dx.doi.org/10.1056/NEJM198810133191503.
18. Hitti J, Krohn MA, Patton DL, Tarczy-Hornoch P, Hillier SL, Cassen EM, Eschenbach DA. 1997. Amniotic fluid tumor necrosis factor-alpha and the risk of respiratory distress syndrome among preterm infants. Am J Obstet Gynecol 177: 50-56. http://dx.doi.org/10.1016/S0002-9378(97)70437-X.
19. Campbell JR, Hillier SL, Krohn MA, Ferrieri P, Zaleznik DF, Baker CJ. 2000. Group B streptococcal colonization and serotype-specific immunity in pregnant women at delivery. Obstet Gynecol 96: 498-503.
20. Allen U, Nimrod C, Macdonald N, Toye B, Stephens D, Marchessault V. 1999. Relationship between antenatal group B streptococcal vaginal colonization and premature labour. Paediatr Child Health 4: 465-469.
21. Stern R, Asari AA, Sugahara KN. 2006. Hyaluronan fragments: an information-rich system. Eur J Cell Biol 85: 699-715. http://dx.doi.org/10.1016/j.ejcb.2006.05.009.
22. Akgul Y, Word RA, Ensign LM, Yamaguchi Y, Lydon J, Hanes J, Mahendroo M. 2014. Hyaluronan in cervical epithelia protects against infection-mediated preterm birth. J Clin Invest 124: 5481-5489. http:// dx.doi.org/10.1172/JCI78765.
23. Akgul Y, Holt R, Mummert M, Word A, Mahendroo M. 2012. Dynamic changes in cervical glycosaminoglycan composition during normal pregnancy and preterm birth. Endocrinology 153: 3493-3503. http:// dx.doi.org/10.1210/en.2011-1950.
24. Mahendroo M. 2012. Cervical remodeling in term and preterm birth: insights from an animal model. Reproduction 143: 429-438. http:// dx.doi.org/10.1530/REP-11-0466.
25. Baker JR, Pritchard DG. 2000. Action pattern and substrate specificity of the hyaluronan lyase from group B streptococci. Biochem J 348: 465-471. http://dx.doi.org/10.1042/bj3480465.
26. Baker JR, Yu H, Morrison K, Averett WF, Pritchard DG. 1997. Specificity of the hyaluronate lyase of group-B streptococcus toward unsulphated regions of chondroitin sulphate. Biochem J 327: 65-71. http:// dx.doi.org/10.1042/bj3270065.
27. Gochnauer TA, Wilson JB. 1951. Hyaluronidase production in vitro by streptococci isolated from bovine mastitis cases. Am J Vet Res 12: 20-22.
28. Kolar SL, Kyme P, Tseng CW, Soliman A, Kaplan A, Liang J, Nizet V, Jiang D, Murali R, Arditi M, Underhill DM, Liu GY. 2015. Group B streptococcus evades host immunity by degrading hyaluronan. Cell Host Microbe 18: 694-704. http://dx.doi.org/10.1016/j.chom.2015.11.001.
29. Greif RL. 1952. Colorimetric determination of hyaluronidase activity. J Biol Chem 194: 619-625.
30. Randis TM, Gelber SE, Hooven TA, Abellar RG, Akabas LH, Lewis EL, Walker LB, Byland LM, Nizet V, Ratner AJ. 2014. Group B streptococcus beta-hemolysin/cytolysin breaches maternal-fetal barriers to cause preterm birth and intrauterine fetal demise in vivo. J Infect Dis 210: 265-273. http://dx.doi.org/10.1093/infdis/jiu067.
31. Musser JM, Mattingly SJ, Quentin R, Goudeau A, Selander RK. 1989. Identification of a high-virulence clone of type III Streptococcus agalactiae (group B streptococcus) causing invasive neonatal disease. Proc Natl Acad Sci U S A 86: 4731-4735. http://dx.doi.org/10.1073/pnas.86.12.4731.
32. Pioli PA, Amiel E, Schaefer TM, Connolly JE, Wira CR, Guyre PM. 2004. Differential expression of Toll-like receptors 2 and 4 in tissues of the human female reproductive tract. Infect Immun 72: 5799-5806. http:// dx.doi.org/10.1128/IAI.72.10.5799-5806.2004.
33. Gonzalez JM, Xu H, Ofori E, Elovitz MA. 2007. Toll-like receptors in the uterus, cervix, and placenta: is pregnancy an immunosuppressed state? Am J Obstet Gynecol 197: 291.e1-296.e6. http://dx.doi.org/10.1016/ j.ajog.2007.06.021.
34. Wang Z, Guo C, Xu Y, Liu G, Lu C, Liu Y. 2014. Two novel functions of hyaluronidase from Streptococcus agalactiae are enhanced intracellular survival and inhibition of proinflammatory cytokine expression. Infect Immun 82: 2615-2625. http://dx.doi.org/10.1128/IAI.00022-14.
35. Hynes WL, Walton SL. 2000. Hyaluronidases of Gram-positive bacteria. FEMS Microbiol Lett 183: 201-207. http://dx.doi.org/10.1111/j.1574-6968.2000.tb08958.x.
36. Girish KS, Kemparaju K. 2007. The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci 80: 1921-1943. http:// dx.doi.org/10.1016/j.lfs.2007.02.037.
37. Ruscheinsky M, De la Motte C, MahendrooM. 2008. Hyaluronan and its binding proteins during cervical ripening and parturition: dynamic changes in size, distribution and temporal sequence. Matrix Biol 27: 487-497. http://dx.doi.org/10.1016/j.matbio.2008.01.010.
38. Straach KJ, Shelton JM, Richardson JA, Hascall VC, Mahendroo MS. 2005. Regulation of hyaluronan expression during cervical ripening. Glycobiology 15: 55-65. http://dx.doi.org/10.1093/glycob/cwh137.
39. Maul H, Mackay L, Garfield RE. 2006. Cervical ripening: biochemical, molecular, and clinical considerations. Clin Obstet Gynecol 49: 551-563. http://dx.doi.org/10.1097/00003081-200609000-00015.
40. Kavanagh J, Kelly AJ, Thomas J. 2006. Hyaluronidase for cervical ripening and induction of labour. Cochrane Database Syst Rev 2: CD003097. http://dx.doi.org/10.1002/14651858.CD003097.pub2.
41. Gendrin C, Vornhagen J, Ngo L, Whidbey C, Boldenow E, Santana-Ufret V, Clauson M, Burnside K, Galloway DP, Waldorf KA, Piliponsky AM, Rajagopal L. 2015. Mast cell degranulation by a hemolytic lipid toxin decreases GBS colonization and infection. Sci Adv 1: e1400225. http:// dx.doi.org/10.1126/sciadv.1400225.
42. 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: 488-505. http://dx.doi.org/10.15252/ emmm.201404883.
43. Spickenreither M, Braun S, Bernhardt G, Dove S, Buschauer A. 2006. Novel 6-O-acylated vitaminCderivatives as hyaluronidase inhibitors with selectivity for bacterial lyases. Bioorg Med Chem Lett 16: 5313-5316. http://dx.doi.org/10.1016/j.bmcl.2006.07.087.
44. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
45. Lancefield RC, McCarty M, Everly WN. 1975. Multiple mouseprotective antibodies directed against group B streptococci. Special reference to antibodies effective against protein antigens. J Exp Med 142: 165-179. http://dx.doi.org/10.1084/jem.142.1.165.
46. Rajagopal L, Clancy A, Rubens CE. 2003. A eukaryotic type serine/ threonine kinase and phosphatase in Streptococcus agalactiae reversibly phosphorylate an inorganic pyrophosphatase and affect growth, cell segregation, and virulence. J Biol Chem 278: 14429-14441. http://dx.doi.org/10.1074/jbc.M212747200.