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Microbe-Induced Epigenetic Alterations

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Patho-Epigenetics of Disease

Abstract

In addition to the DNA and RNA tumor viruses affecting the epigenotype of their host cells (see 8), certain viruses which are not directly involved in tumorigenesis interact with the cellular epigenetic regulatory mechanisms, as well. In CD4+ T cells, human immunodeficiency virus infection downregulates interferon-gamma (IFN-γ) expression by inducing de novo methylation of the IFN-γ promoter and silences a tumor suppressor gene (p16INK4A) and the gene coding for N-acetylmannosamine kinase (GNE), a key enzyme in sialylation of surface glycoproteins, in a similar manner. Infection of nonneoplastic cells by hepatitis C virus, a tumor-associated virus, results in epigenetic silencing of IFN-α responsive genes, an effect that influences the success of antiviral therapy, but is not necessarily related to hepatocarcinogenesis. During lytic infection, the immediate-early proteins of human cytomegalovirus block the activity of cellular histone deacetylases (HDACs), facilitating productive virus replication. Pathogenic bacteria, including Listeria monocytogenes, Streptococcus pneumoniae, Clostridium perfringens, and Aeromonas hydrophila produce toxins that alter modified histones or secrete butyric acid, a HDAC inhibitor, like Porphyromonas gingivalis, a causative agent of periodontal disease. Others, as exemplified by Shigella flexneri, Anaplasma phagocytophilum, and Mycobacterium tuberculosis, synthesize effector proteins that change the pattern of histone modifications around host defense gene promoters, facilitating immune evasion. In principle, the protein methyltransferases of Chlamydia trachomatis and Chlamydophila pneumoniae may also elicit epigenetic reprogramming in infected cells by methylating host histones. Hypermethylation of cellular promoters may be the patho-epigenetic mechanism resulting in intrauterine growth restriction in association with Campylobacter rectus infection. Uropathogenic Escherichia coli can also induce CpG methylation at distinct cellular promoters in vitro. Similarly, profound alterations in the methylation pattern of the host cell DNA accompany the development of gastric carcinoma in Helicobacter pylori-infected individuals. Pathogenic protozoa use their own epigenetic regulatory mechanisms to control virulence gene expression and differentiation. Although their influence on the host cell epigenome remains to be elucidated at greater depth, the unique features of the protozoan epigenetic machineries may provide excellent targets for novel therapeutic drugs.

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Abbreviations

actA:

Gene of actin assembly-inducing protein

AID:

Activation-induced cytidine deaminase

AIDS:

Acquired immunodeficiency syndrome

ARC:

AIDS-related complex

BL:

Burkitt’s lymphoma

BMDC:

Bone marrow-derived cell

CagA:

Cytotoxicity-associated antigen

CBF1:

C promoter-binding factor 1, also termed RBP-Jκ

CGI:

CpG island

CIITA:

Class II transactivator

CSF1R:

Colony-stimulating factor 1 receptor

CTF:

CCAAT box-binding transcription factor

DNMT:

DNA methyl transferase

EB:

Elementary body

EhMLBP:

Entamoeba histolytica-methylated LINE-binding protein

EMT:

Epithelial–mesenchymal transition

ERF:

Ets-2 repressor factor

ES:

Expression site

ESB:

ES body

flaA:

Flagellin A gene

GC:

Gastric carcinoma

H3K27me3:

Histone 3 trimethylation at lysine 27

H3K4me2:

Histone 3 dimethylation at lysine 4

H3K4me3:

Histone 3 trimethylation at lysine 4

H3S10:

Histone 3 serine 10

H3S10pho:

Histone 3 phosphorylation at serine 10

H4K16ac:

Histone 4 acetylation at lysine 16

H4K20me3:

Histone 4 trimethylation at lysine 20

H4R3me2:

Histone 4 dimethylation at arginine 3

HAART:

Highly active antiretroviral therapy

Hc1:

Chlamydial histone-like protein

HCMV:

Human cytomegalovirus

HCV:

Hepatitis C virus

HDAC:

Histone deacetylase

HIV:

Human immunodeficiency virus

HL:

Hodgkin’s lymphoma

hly:

Listeriolysin O gene

HP:

Heterochromatin protein

Hp:

Helicobacter pylori

HRF:

HIV reactivating factor

IE:

Immediate-early

Igf2:

Insulin-like growth factor 2

IL:

Interleukin

inlC:

Internalin C gene

JNK:

c-Jun NH2-terminal kinase

LINE:

Long interspersed nuclear element

LLO:

Listeriolysin O

lncRNA:

Long noncoding RNA

LTR:

Long terminal repeat

MAF:

Musculoaponeurotic fibrosarcoma

MBD2:

Methyl-CpG-binding protein 2

MIEP:

Major immediate-early promoter

MPL:

Metalloproteinase

NHL:

Non-Hodgkin’s lymphoma

NO:

Nitric oxide

NUE:

Nuclear effector

OspF:

Outer Shigella protein F

PCNSL:

Primary central nervous system lymphoma

PD:

Periodontal disease

PFO:

Perfringolysin O

PLY:

Pneumolysin

PP2A:

Protein phosphatase 2A

PRC:

Polycomb repressive complex

PRMT1:

Protein arginine methyltransferase 1

PU.1:

Purine-rich box-1

RB:

Reticulate body

RT:

Reverse transcriptase

SAHA:

Suberoylanilide hydroxamic acid

SAM:

S-Adenosyl-l-methionine

SH2:

Src homology 2

SHP2:

SH2-containing tyrosine phosphatase

SPEM:

Spasmolytic polypeptide-expressing metaplasia

TBP:

TATA-binding protein

TLR:

Toll-like receptor

TNFα:

Tumor necrosis factor-alpha

TpSCOP:

Theileria parva schizont-derived cytoskeleton-binding protein

TSA:

Trichostatin A

uhpT:

Glucose-6P permease gene

UPEC:

Uropathogenic Escherichia coli

VacA:

Vacuolating cytotoxin

VPA:

Valproic acid

Vpr:

Viral protein R

VSG:

Variant surface glycoprotein

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  1. Institute for Medical Microbiology and Hygiene, University of Regensburg, Regensburg, Germany

    Hans Helmut Niller MD

  2. Microbiological Research Group, National Center for Epidemiology, Budapest, Hungary

    Ferenc Banati, Eva Ay & Janos Minarovits MD, MSc

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  1. Hans Helmut Niller MD
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  1. Microbiological Research Group, National Center for Epidemiology, Piheno u. 1, Budapest, 1529, Hungary

    Janos Minarovits

  2. University of Regensburg, Regensburg, 93053, Germany

    Hans Helmut Niller

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Niller, H.H., Banati, F., Ay, E., Minarovits, J. (2012). Microbe-Induced Epigenetic Alterations. In: Minarovits, J., Niller, H. (eds) Patho-Epigenetics of Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3345-3_14

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