Variation in Macrophage Phagocytosis of Streptococcus agalactiae Does Not Reflect Bacterial Capsular Serotype, Multilocus Sequence Type or Association with Invasive Infection

Article Sidebar

Pathogens and Immunity Vol3, No1
HTML PDF
Published: May 18, 2018
DOI: https://doi.org/10.20411/pai.v3i1.233
Keywords:
Neonatal sepsis, , innate immunity, macrophages, Gram positive bacteria, diabetes, macrophage, bacterial infection, encapsulated bacteria, immunology

Main Article Content

Lisa M. Rogers
Division of Infectious Diseases, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee
Jennifer A. Gaddy
Division of Infectious Diseases, Department of Medicine, Department of Pathology, Vanderbilt University Medical Center, Nashville, Tennessee; Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee
Shannon D. Manning
Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan
http://orcid.org/0000-0001-9581-0660
David M. Aronoff
Director, Division of Infectious Diseases Department of Medicine, Vanderbilt University Medical Center
http://orcid.org/0000-0003-4587-6121

Abstract

Background: Group B Streptococcus(GBS) is an encapsulated Gram-positive coccus that is an important cause of infections in adults with chronic medical conditions, pregnant women, and neonates. GBS causes a range of clinical syndromes, from asymptomatic colonization to deep-seated invasive and highly lethal infections. Macrophages are important sentinels of innate immunity, protecting host tissues from infection when bacteria advance beyond cutaneous or mucosal barriers. We hypothesized that the capacity for macrophages to phagocytose unopsonized GBS would vary across distinct clinical strains, and such differences would reflect serotype diversity.

Methods: A high-throughput screen using the phorbol ester-differentiated THP-1 macrophage-like human cell line was used to quantify phagocytosis of a diverse group of 35 different human clinical isolates of GBS representing a wide variety of capsular serotypes. Validation studies were conducted using human primary phagocytes.

Results: Phagocytosis of GBS differed widely across clinical isolates but this was not related to capsular serotype, genetic sequence type, pilus type, or clinical source of the GBS isolate (colonizing or invasive strain).

Conclusions: Structural and/or biochemical differences among diverse GBS strains are reflected in a diverse capacity for macrophages to ingest them through non-opsonic phagocytosis. Mechanisms explaining these differences are not clear.

Keywords: Neonatal sepsis; innate immunity; macrophages; Gram-positive bacteria; diabetes

Downloads

Download data is not yet available.

Article Details

Issue
Vol. 3 No. 1: Volume 3, Number 1
Section
Articles

Pathogens and Immunity abides by Creative Commons BY 4.0:

http://creativecommons.org/licenses/by/4.0/

This license lets others distribute, remix, tweak, and build upon your work for any lawful purpose, even commercially, as long as they credit you for the original creation. This is the most accommodating of licenses offered. Recommended for maximum dissemination and use of licensed materials. The authors maintain copyright of their materal.

*Due to a template error on our pdfs, articles published from May 20, 2016 to June 24, 2022 incorrectly state the copyright is held by Pathogens and Immunity. Copyright of all articles is held by the authors of each article as noted in the above copyright policy.   

Crossref
Scopus
Google Scholar
Europe PMC

References

1. Phares CR, Lynfield R, Farley MM, Mohle-Boetani J, Harrison LH, Petit S, Craig AS, Schaffner W, Zansky SM, Gershman K, Stefonek KR, Albanese BA, Zell ER, Schuchat A, Schrag SJ. Active Bacterial Core surveillance/Emerging Infections Program N. Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005. JAMA. 2008;299(17):2056-65. PubMed PMID: 18460666. doi: 10.1001/jama.299.17.2056

2. Randis TM, Baker JA, Ratner AJ. Group B Streptococcal Infections. Pediatrics in Review. 2017;38(6):254-62. doi:10.1542/pir.2016-0127

3. Seale AC, Bianchi-Jassir F, Russell NJ, Kohli-Lynch M, Tann CJ, Hall J, Madrid L, Blencowe H, Cousens S, Baker CJ. Estimates of the burden of group B streptococcal disease worldwide for pregnant women, stillbirths, and children. Clinical Infectious Diseases. 2017;65(suppl_2):S200-S19.

4. Patras KA, Nizet V. Group B Streptococcal Maternal Colonization and Neonatal Disease: Molecular Mechanisms and Preventative Approaches. Frontiers in Pediatrics. 2018;6:27.

5. Fabbrini M, Rigat F, Rinaudo CD, Passalaqua I, Khacheh S, Creti R, Baldassarri L, Carboni F, Anderloni G, Rosini R, Maione D, Grandi G, Telford JL, Margarit I. The Protective Value of Maternal Group B Streptococcus Antibodies: Quantitative and Functional Analysis of Naturally Acquired Responses to Capsular Polysaccharides and Pilus Proteins in European Maternal Sera. Clinical Infectious Diseases. 2016;63(6):746-53. doi: 10.1093/cid/ciw377

6. Marques MB, Kasper D, Pangburn M, Wessels M. Prevention of C3 deposition by capsular polysaccharide is a virulence mechanism of type III group B streptococci. Infection and Immunity. 1992;60(10):3986-93.

7. Tsuchiya S, Kobayashi Y, Goto Y, Okumura H, Nakae S, Konno T, Tada K. Induction of Maturation in Cultured Human Monocytic Leukemia-Cells by A Phorbol Diester. Cancer Research. 1982;42(4):1530-6.

8. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). International Journal of Cancer. 1980;26(2):171-6. doi: 10.1002/ijc.2910260208

9. Mason KL, Rogers LM, Soares EM, Bani-Hashemi T, Erb-Downward J, Agnew D, Peters-Golden M, Weinberg JB, Crofford LJ, Aronoff DM. Intrauterine group A streptococcal infections are exacerbated by prostaglandin E2. J Immunol. 2013;191(5):2457-65. PubMed PMID: 23913961. Pubmed Central PMCID: 3750066. doi: 10.4049/jimmunol.1300786

10. Soares EM, Mason KL, Rogers LM, Serezani CH, Faccioli LH, Aronoff DM. Leukotriene B4 enhances innate immune defense against the puerperal sepsis agent Streptococcus pyogenes. J Immunol. 2013;190(4):1614-22. PubMed PMID: 23325886. Pubmed Central PMCID: 3563855. doi: 10.4049/jimmunol.1202932

11. Davies HD, Raj S, Adair C, Robinson J, McGeer A, Alberta GBSSG. Population-based active surveillance for neonatal group B streptococcal infections in Alberta, Canada: implications for vaccine formulation. Pediatr Infect Dis J. 2001;20(9):879-84. PubMed PMID: 11734768.

12. Spaetgens R, DeBella K, Ma D, Robertson S, Mucenski M, Davies HD. Perinatal antibiotic usage and changes in colonization and resistance rates of group B streptococcus and other pathogens. Obstet Gynecol. 2002;100(3):525-33. PubMed PMID: 12220773.

13. Aronoff DM, Canetti C, Peters-Golden M. Prostaglandin E2 inhibits alveolar macrophage phagocytosis through an E-prostanoid 2 receptor-mediated increase in intracellular cyclic AMP. J Immunol. 2004;173(1):559-65. PubMed PMID: 15210817.

14. Manning SD, Springman AC, Lehotzky E, Lewis MA, Whittam TS, Davies HD. Multilocus sequence types associated with neonatal group B streptococcal sepsis and meningitis in Canada. J Clin Microbiol. 2009;47(4):1143-8. PubMed PMID: 19158264.

15. Springman AC, Lacher DW, Waymire EA, Wengert SL, Singh P, Zadoks RN, Davies HD, Manning SD. Pilus distribution among lineages of group b Streptococcus: an evolutionary and clinical perspective. BMC Microbiol. 2014;14:159. PubMed PMID: 24943359. Pubmed Central PMCID: PMC4074840. doi: 10.1186/1471-2180-14-159

16. Kothary V, Doster RS, Rogers LM, Kirk LA, Boyd KL, Romano-Keeler J, Haley KP, Manning SD, Aronoff DM, Gaddy JA. Group B Streptococcus Induces Neutrophil Recruitment to Gestational Tissues and Elaboration of Extracellular Traps and Nutritional Immunity. Front Cell Infect Microbiol. 2017;7:19. PubMed PMID: 28217556. Pubmed Central PMCID: PMC5289994. doi: 10.3389/fcimb.2017.00019

17. Singh P, Aronoff DM, Davies HD, Manning SD. Draft Genome Sequence of an Invasive Streptococcus agalactiae Isolate Lacking Pigmentation. Genome Announc. 2016;4(1). PubMed PMID: 26950320. Pubmed Central PMCID: PMC4767910. doi: 10.1128/genomeA.00015-16

18. Gendrin C, Vornhagen J, Armistead B, Singh P, Whidbey C, Merillat S, Knupp D, Parker R, Rogers LM, Quach P, Iyer LM, Aravind L, Manning SD, Aronoff DM, Rajagopal L. A Nonhemolytic Group B Streptococcus Strain Exhibits Hypervirulence. J Infect Dis. 2018;217(6):983-7. PubMed PMID: 29244079. doi: 10.1093/infdis/jix646

19. Korir ML, Laut C, Rogers LM, Plemmons JA, Aronoff DM, Manning SD. Differing mechanisms of surviving phagosomal stress among group B Streptococcus strains of varying genotypes. Virulence. 2017;8(6):924-37. PubMed PMID: 27791478. Pubmed Central PMCID: PMC5626345. doi: 10.1080/21505594.2016.1252016

20. Montenegro-Burke JR, Sutton JA, Rogers LM, Milne GL, McLean JA, Aronoff DM. Lipid profiling of polarized human monocyte-derived macrophages. Prostaglandins and Other Lipid Mediators. 2016;In press.

21. Chang YC, Olson J, Louie A, Crocker PR, Varki A, Nizet V. Role of macrophage sialoadhesin in host defense against the sialylated pathogen group B Streptococcus. J Mol Med (Berl). 2014;92(9):951-9. PubMed PMID: 24788876. Pubmed Central PMCID: 4133643. doi: 10.1007/s00109-014-1157-y

22. Chattopadhyay D, Carey AJ, Caliot E, Webb RI, Layton JR, Wang Y, Bohnsack JF, Adderson EE, Ulett GC. Phylogenetic lineage and pilus protein Spb1/SAN1518 affect opsonin-independent phagocytosis and intracellular survival of Group B Streptococcus. Microbes Infect. 2011;13(4):369-82. PubMed PMID: 21238599. S1286-4579(11)00019-0 [pii] doi: 10.1016/j.micinf.2010.12.009

23. Ralph P, Nakoinz I. Phagocytosis and cytolysis by a macrophage tumour and its cloned cell line. Nature. 1975;257(5525):393-4. PubMed PMID: 1101071.