Journal of
Endocrinology and Thyroid Research
ISSN: 2573-2188
Review Article
J Endocrinol Thyroid Res
Volume 2 Issue 5 - November 2017
DOI: 10.19080/JETR.2017.02.555598
Copyright © All rights are reserved by Primrose Freestone
Microbe-Endocrine Hormone Interactions
Shamim Al-Husseini, Abdalla Hamed and Primrose Freestone*
Department of Infection, Immunity and Inflammation, University Road, UK
Submission: October 10, 2017; Published: December 14, 2017
*Corresponding author: Primrose Freestone, Department of Infection, Immunity and Inflammation, Maurice Shock Medical Sciences Building,
; Fax: +44 (0)116-252-5030; Email:
University of Leicester, University Road, Leicester LE1 9HN UK, Tel:
Introduction
The influence of hormones on human cells is very well
characterized, yet much less understood is the response to those
chemical signals of the 1013-1014 bacteria and fungi that are coresident within the human frame [1]. Microbial Endocrinology is
a research area which seeks to understand the role of microbial
interactions with mammalian hormones in conditions of health
and disease [2-4]. It takes the view that through their long
evolutionary relationship with animals microorganisms have
evolved systems for sensing hormones which they use as an
indicator that they are within the proximity of a potential host.
This article considers what happens when the human microbiota
Table 1: Hormone responsive microorganisms.
come into contact with the chemical signals of their host, and the
health significance of this inter-kingdom-encounter.
Hormones can be classified on the basis of their chemical
structures: amino acid, peptide and protein and cholesterol
based, and the receptor location by which the hormonal signal
is transduced. The function of each hormonal type will be
described, and the health implications to the host when the
hormone is encountered by potentially infectious bacteria and
fungi. Structures of the hormones covered and the microbes
which recognize them can be found in Table 1, respectively [539].
Species
Hormone/Metabolite
Growth
Virulence
Reference
Aeromonas hydrophila
NE
+
+
Kinney et al. [5]
+
Anderson & Armstrong [7]
Acinetobacter lwoffii
NE
+
Bordetella bronchiseptica,B. pertussis
NE, Adr, Dop
+
Borrelia burgdorferi
NE
Brachyspira pilosicoli
NE
+
+
Campylobacter jejuni
NE
+
+
Citrobacterfreundii, C. rodentium
NE
+
Enterobacter agglomerans, E. sakazaki
NE
+
Enterococcus faecalis, E. cloacae
NE
+
Escherichia coli (commensal and pathogenic)
NE, Adr, Dop, Iso, Dob,
DHPG, DHMA
Hafnia alvei
NE
+
+
Helicobacter pylori
NE
+
NE
+
Listeria monocytogenes
NE, Adr, Dop
+
+
Morganella morgana
NE
Mycoplasma hyponeumoniae
NE
Proteus mirabilis
NE
J Endocrinol Thyroid Res 2(5): JETR.MS.ID.555598 (2017)
Cogan et al. [10]
Freestone et al. [6]
Freestone et al. [6]
+
Lyte & Ernst [12], Freestone et
al. [6,13-15], Green et al. [16],
Vlisidou et al. [17], Sandrini et al.
[18]
Freestone et al. [6]
Doherty et al. [19]
Freestone et al. [6]
Coulanges et al. [20], Freestone
et al. [6]
+
+
Scheckelhoff et al. [8]
Naresh & Hampson [9]
Freestone et al. [6], Bailey et al.
[11]
+
Klebsiella oxytoca, K. pneumoniae
Freestone et al. [6]
Freestone et al. [6]
O’Neal et al. [21]
Freestone et al. [6]
001
Journal of Endocrinology and Thyroid Research
Pseudomonas aeruginosa
NE, Adr, Dop
+
+
Salmonella enterica, Salmonella Typhimurium
NE, Adr, Dop
+
+
Shigella sonnei, S. flexneri
NE
+
Staphylococcus aureus
NE, Dop
+
S. saprophyticus, S. haemolyticus, S. hominis
NE, Adr, Dop, Iso, Dob
+
Streptococcus dysgalactica
NE
+
NE, Adr, Dop
+
Xanthomonas maltophila
NE
+
Yersinia enterocolitica
NE, Adr, Dop,
+
Periodontal pathogens
NE, Adr
+
Freestone et al. [27]
+
+
Insulin
Candia albicans
Oestrogen
Freestone et al. [6,27]
Freestone et al. [6]
Nakano et al. [28]
Freestone et al. [6]
Freestone et al. [6,29]
Roberts et al. [30]
Actinomyces gerenscseriae, A. naeslundii, A.
odontolyticus, Campylobacter gracilis, Capnocytophaga sputigena, C. gingivalis, Eikenella
corrodens, Eubacterium saburreum, Fusobacterium periodonticum, F. nucleatum subsp. Vincentii,
Leptotrichia buccalis, Neisseria mucosa, Peptostreptococcus anaerobius, P. micros, Prevotella
denticola, P. Melaninogenica, S. intermedius, S.
gordonii, S. constellatus, S. mitis, S. mutans, S.
sanguis
Burkholderia pseudomallei
Freestone et al. [6,24] Methner et
al. [25], Pullinger et al. [26]
Freestone et al. [6,27]
Staphylococcus epidermidis, S. capitis,
Vibrio parahaemolyticus, V. mimicus, V. vulnificus
Alverdy et al.[22], Freestone et al.
[6,23]
+
Wood et al. [31]
+
Schreiber & Brown [39]
Progesterone
Luteinising hormone
+
+
+
+
+
Banerjee et al. [35]
Kinsman et al. [32],
White & Larsen [33],
Tarry et al. [34]
Bramley et al. [36,37]
Chlamydia trachomatis
Oestrogen
Progesterone
+
Sonnex [38]
Sonnex [38]
E. coli
ACTH
+
The ‘+’ indicates that the hormone shown, or their metabolites have induced enhancement of growth or virulence of the bacterial
species shown. Key: NE, noradrenaline; Adr, adrenaline; Dop, dopamine; Iso, isoprenaline; Dob, dobutamine; DHPG, dihydroxy
phenylglycol; DHMA, dihydroxy mandelic acid, ACTH, adrenocorticotrophic hormone.
This table was adapted with permission from Freestone [3].
Amino Acid-Derived Hormones
These are commonly derived from dietary tyrosine and
tryptophan, and comprise two main types: thyroid hormone such
as thyroxine and the catecholamines dopamine, noradrenaline
and adrenaline [5]. Catecholamines are well studied as they
possess a diversity of signaling functions and are widely
002
distributed throughout the tissues and organs of the human
body [5]. Noradrenaline and adrenaline are neurotransmitters
but also play an integral role in the flight or fight response. In
terms of the infection significance of catecholamine release,
the field of psychoneuroimmunology has long reported that
stress hormone elevations in humans and animals increases
their risk of developing an infection. This is in part due to
How to cite this article: Shamim Al-H, Abdalla H, Primrose F. Microbe-Endocrine Hormone Interactions. J Endocrinol Thyroid Res . 2017; 2(5): 5555978.
DOI: 10.19080/JETR.2017.02.555598
Journal of Endocrinology and Thyroid Research
stress-released catecholamine and glucocorticoid hormones
reducing the functionality of the immune system [6,7]. More
recently, Microbial Endocrinology studies have shown that
like immune cells many bacteria involved in human infections
recognize catecholamines which they appear to use as an
indicator that their host is stressed, and possibly less able to
mount a defense to the invading microbe [3,4]. Table 1 shows the
catecholamine-responsive microbes that have been identified so
far. Most analyses of bacterial stress hormone interactions have
looked at growth effects using serum- or blood-based culture
media, chosen to more closely reflect the host environment in
which the hormone will be encountered [40]. Blood or serum
containing media is iron limited due to the presence of ferric
iron sequestering proteins such as transferrin or lactoferrin
which inhibits the growth of most bacterial pathogens [41].
Because iron is so essential for the in-vivo growth of bacteria
[42], its limitation by transferrin and lactoferrin represents a key
immune defense against infection. However, bacteria can directly
use catecholamines as a kind of siderophore to steal transferrin
and lactoferrin Fe which enables up to 100,000-fold increases
in bacterial cell numbers in what normally should be highly
bacteriostatic host tissue fluids [14,15,18,23].
Dopamine, noradrenaline and adrenaline exposure can also
induce pathogenic bacteria to become even more virulent by
inducing expression of genes in toxin release [43], increasing
biofilm formation [18] and enhancing attachment to host
epithelial tissues [16,17]. Catecholamines can even catalyze
recovery of bacteria severely damaged by antibiotic treatment
[18,27], and rapidly promote exchange of genetic material
between different bacterial species [44]. In terms of the
infection significance of catecholamine-microbe interactions,
catecholamines are used therapeutically in acutely ill patients
to maintain heart and kidney function [5]. Catecholamines at
the levels infused down intravenous catheter lines were found
to massively increase staphylococcal biofilm formation on the
same plastic, while clinically attainable levels of catecholamines
also increased P. aeruginosa biofilm formation on endotracheal
tubing (used to maintain an open airway in ventilated patients)
as well as enabling the pathogen to resist antibiotic treatment
[18].
Peptide and Protein Hormones
There are reports of peptide-like hormones affecting the
infectious potential of pathogenic bacteria. Melioidosis is an
infectious disease caused by the Gram-negative bacterium
Burkholderia pseudomallei, which tends to be found in soil
and water of tropical climates such as Vietnam and parts of
Australia. It has been observed that type I diabetes mellitus is
an apparent risk factor for the development of the septicemic
form of melioidosis [20]. Woods and co-workers found that B.
pseudomallei can directly bind human insulin and that each
bacterial cell expressed around 5000 surface-associated insulin
receptors. Woods et al. [31] showed that insulin inhibited the
growth of B. pseudomallei and suggested that the deficiency
003
of the hormone at least in part explained the higher risk of
melioidosis in insulin-dependent diabetics [31].
Adrenocorticotropic hormone (ACTH) is a peptide hormone
that induces the adrenal cortex to produce corticosteroid
hormones such as cortisol which contribute to regulation of
systemic glucose levels. It is therefore interesting that Schreiber
and Brown found that exposure to ACTH increased attachment
of E. coli O157:H7 to gut epithelia, though the underlying
mechanism for this response is not clear [39]. Thyrotropin is
a pituitary hormone that induces the thyroid gland to produce
thyroxine followed by triiodothyronine which stimulates
oxidative respiration and organ development. Interestingly,
use of radiolabelled thyrotropin has showed the presence of
receptor for thyrotropin in Yersinia enterocolitica [45,46]. The
thyrotropin specificity of the Y.enterocolitica binding activity
was similar to that of the thyrotropin receptor in human thyroid
tissue. This binding activity is thought to have implications
for Graves’ disease, which is an autoimmune disease in which
thyroid-stimulating antibodies to the thyroid-stimulating
hormone receptor mimic thyroid-stimulating hormone, which
activates the receptor leading to hyperthyroidism. Thyrotropin
binding sites on have been shown to be recognized by antibodies
from humans with Graves’ disease, and prior infection by Y.
enterocolitica has been implicated in the pathogenesis of Graves’
disease [46]. The outer membrane porins Omp A,C and F have
been identified as the Y. enterocolitica targets recognized by
Graves’ patient antibodies, though their role in contributing to
development of Graves’ disease remains to be shown [47].
Candida albicans is a dimorphic opportunistic fungal
pathogen of females and the immunocompromised which has
been shown to interact with several human peptide hormones.
Luteinizing hormone is required for ovulation and the formation
of a corpus luteum in the female menstrual cycle. C. albicans has
been shown to bind human luteinizing hormone and chorionic
gonadotropin [36]. Bramley et al. [36] used (125I)-labeled
luteinizing hormone and chorionic gonadotropin to demonstrate
the presence of specific binding sites for both hormones in C.
albicans, and C. tropicalis [36]. The binding activity was found to
be highly specific and was not surface associated instead being at
greatest levels in microsomes and cytoplasmic fractions. Also, of
considerable relevance to C. albicans infectivity, interaction with
the luteinizing hormone was found to stimulate germination of
Candida spores and germ tube formation [32].
Cholesterol-Derived Hormones
Cholesterol is the chemical basis of steroid hormones such as
oestrogen, progesterone and testosterone which regulate aspects
of the metabolism, tissue differentiation and reproductive
cycles of females and males. Investigations from a variety of
researchers have shown that exposure of some bacteria and fungi
to steroid hormones can elevate infection risk in certain patient
groups. For instance oestrogen have been shown to increase
the likelihood of urogenital infections, particularly during
How to cite this article: Shamim Al-H, Abdalla H, Primrose F. Microbe-Endocrine Hormone Interactions. J Endocrinol Thyroid Res . 2017; 2(5): 5555978.
DOI: 10.19080/JETR.2017.02.555597
Journal of Endocrinology and Thyroid Research
pregnancy, or in women taking high oestrogen contraceptives
or hormone replacement therapy [38]. Chlamydia trachomatis is
an important sexually transmitted pathogen, especially in young
women; Sonnex [38] reported that treatment of C. trachomatis
with physiological levels of oestrogen increased infection of
human endometrial cells, and enhanced Chlamydia colonisation
of female mice. C. trachomatis infection of female mice was also
increased following pre-treatment with progesterone. C. albicans
is a major source of fungal infections in women of reproductive
age [38] which has been shown to possess an oestrogen binding
protein of high affinity and specificity [32,33,34]. Contact with
oestrogen has been reported to increase C. albicans growth as
well as its infectivity, causing the yeast to shift into to a more
invasive hyphal morphology [33]. Tarry et al. [34] showed that
C. albicans vaginal colonization in a rat model of infection was
increased over 8-fold when a physiological level of oestrogen
was present [38]. Banerjee et al. [35] investigated the effects
of progesterone on C. albicans gene expression and found
that expression of 99 genes was differentially affected by the
hormone. Most changes were metabolism associated such as
protein synthesis and cellular transport. Of relevance to infection
risk was the finding that expression of virulence associated
genes such as those involved in hyphal induction, pathogenesis
and multi-drug resistance genes were significantly increased in
progesterone-treated Candida [48-50].
3. Freestone P (2013) Communication between bacteria and their hosts.
Scientifica 2013: 361073.
The effects of endogenous hormones on mammalian cell are
well understood, yet although microbes within the human body
will repeatedly encounter their host hormones the biological
significance to the host of these interactions is only now
becoming apparent. This review examined only a few of the many
hormones within the human body, but still revealed that there
are considerable health implication for some of the microbehormone encounters. Table 1 revealed that the most extensively
studied area of microbial endocrinology is catecholaminerelated, largely because of the long held view of stress increasing
infection risk. However it is clear that other types of contact the
human microbiota may have with mammalian hormones has
health implications. It will be interesting to discover if additional
signals within our hormonal milieu are being sensed by the
thousands of other species of microbes we host.
13. Freestone PP, Williams PH, Haigh RD, Maggs AF, Neal CP, et al. (2002)
Growth stimulation of intestinal commensal Escherichia coli by
catecholamines: a possible contributory factor in trauma-induced
sepsis. Shock 18(5): 465-470.
Conclusion
Acknowledgement
SA gratefully acknowledges the funding of the Iraqi
Government High Committee Education Development in Iraq
HCED. AH acknowledges the support of the Ministry of Higher
Education, Libyan Government.
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DOI: 10.19080/JETR.2017.02.555598
Journal of Endocrinology and Thyroid Research
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How to cite this article: Shamim Al-H, Abdalla H, Primrose F. Microbe-Endocrine Hormone Interactions. J Endocrinol Thyroid Res . 2017; 2(5): 5555978.
DOI: 10.19080/JETR.2017.02.555597
Journal of Endocrinology and Thyroid Research
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How to cite this article: Shamim Al-H, Abdalla H, Primrose F. Microbe-Endocrine Hormone Interactions. J Endocrinol Thyroid Res . 2017; 2(5): 5555978.
DOI: 10.19080/JETR.2017.02.555598