Rapidly Growing Mycobacterium Species: The Long and Winding Road from Tuberculosis Vaccines to Potent Stress-Resilience Agents
Abstract
:1. Introduction
1.1. The “Old Friends” Hypothesis: A Biological Concept to Explain the Increasing Prevalence Rates of Stress-Associated Inflammatory Disorders in Modern Urban Societies
1.2. Mycobacterium vaccae NCTC 11659: General Information
2. History of Mycobacterium vaccae NCTC 11659 Research
2.1. Observational Studies on the Protective Effects of M. vaccae NCTC 11659 and M. vaccae ATCC 15483T: Chronological Evidence
2.1.1. M. vaccae NCTC 11659 and TB
Single Intradermal M. vaccae NCTC 11659 Administration as an Adjunct Therapy for First-Line Drug Therapy for Treatment of TB
Repeated Intradermal M. vaccae NCTC 11659 Administrations as an Adjunct Therapy for First-Line Drug Therapy for Treatment of TB
Repeated Oral M. vaccae NCTC 11659 Administrations Promote Treatment of TB
Repeated Intradermal M. vaccae NCTC 11659 Administration Prevents TB in Persons with HIV Infection
2.1.2. M. vaccae NCTC 11659 and Leprosy
2.1.3. M. vaccae NCTC 11659 and Psoriasis
2.1.4. M. vaccae NCTC 11659 and Atopic Dermatitis
2.1.5. M. vaccae NCTC 11659 and Asthma
2.1.6. M. vaccae NCTC 11659 and Cancer
2.2. Mechanistic Studies on the Protective Effects of M. vaccae NCTC 11659 and M. vaccae ATCC 15483T
2.2.1. M. vaccae NCTC 11659 Effects on DCs and Th1/Th2 Immune Profile
2.2.2. M. vaccae NCTC 11659 Effects on γδ T Cells
2.2.3. M. vaccae NCTC 11659 Effects on CD11b+ Myeloid Cells
2.2.4. M. vaccae ATCC 15483T Effects on CD8+ CTL
2.2.5. M. vaccae NCTC 11659 Effects on Tregs
2.2.6. M. vaccae NCTC 11659 Effects on Brain Microglia
2.2.7. M. vaccae ATCC 15483T Effects on Gene Expression in the Context of TB Infection
3. The Route of M. vaccae NCTC 11659 Administration Affects Its Immunoregulatory Effects
3.1. Invasive Route: s.c. Administration of M. vaccae NCTC 11659 and M. vaccae ATCC 15483T
3.2. Non-Invasive Routes of Administration of M. vaccae NCTC 11659
3.2.1. i.n. Administration of M. vaccae NCTC 11659
3.2.2. i.g./p.o. Administration of M. vaccae NCTC 11659
4. Summary and Conclusions
- Preparations of M. vaccae NCTC 11659 have been shown, regardless of their administration route, to have immunomodulatory properties (for summary see Figure 1).
- Preparations of M. vaccae NCTC 11659 have been shown to be beneficial in a plethora of conditions such as TB, leprosy, psoriasis, dermatitis, allergy, asthma, and several cancers as well as inescapable and chronic psychosocial stress.
- While invasive s.c. and non-invasive i.g. administration of M. vaccae NCTC 11659 mediate their protective effects at least in part via induction of Tregs, the non-invasive i.n. administration of M. vaccae NCTC 11659 protects against the negative pro-inflammatory consequences of chronic psychosocial stress without affecting splenic and mesLN Treg counts.
5. Future Perspectives
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
10(Z)-HDA | 10(Z)-hexadecenoic acid |
ACTH | adrenocorticotropic hormone |
ART | antiretroviral therapy |
ATCC | American Type Culture Collection, Manassas, VA, USA |
AUC | area under the curve |
BAL | bronchoalveolar lavage |
BBS | borate-buffered saline |
BCG | Bacillus Calmette Guérin |
CCL2 | C–C motif chemokine ligand 2, also referred to as monocyte chemoattractant protein-1 (MCP-1) |
CD | cluster of differentiation |
CECT | Colección Española de Cultivos Tipo |
CFU | colony-forming units |
CCUG | Culture Collection |
University of Goteborg | Sweden |
CLR | C-type lectin receptor |
COVID-19 | coronavirus disease 19 |
CREB | cAMP-response element binding protein |
CSC | chronic subordinate colony housing |
CTL | cytotoxic T lymphocyte |
CXCL2 | C-X-C motif chemokine ligand 2 |
DC | dendritic cell |
DSM | DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH |
Braunschweig | Germany |
DSS | dextran sulfate sodium |
ESR | erythrocyte sedimentation rate |
EZM | elevated zero-maze |
FoxP3 | forkhead box protein P3 |
GM-CSF | granulocyte-macrophage colony-stimulating factor |
GYM | Glucose, yeast, and malt agar |
HIV | human immunodeficiency virus |
HPA | hypothalamic-pituitary-adrenal |
hsp | heat-shock protein |
i.d. | intradermal |
IFNγ | interferon gamma |
i.g. | intragastric |
Ig | immunoglobulin |
i.m. | intramuscular |
i.n. | intranasal |
KCTC | Korean Collection of Type Cultures |
IL | interleukin |
INH | isonicotinic acid hydrazide (isoniazid) |
IPT | INH preventative therapy |
i.t. | intratracheal |
LPS | lipopolysaccharide |
MAPK | mitogen-activated protein kinase |
MB7H10 | middlebrook 7H10 agar |
M cells | microfold cells |
MCP-1 | monocyte chemoattractant protein-1, also referred to as C-C motif chemokine ligand 2 (CCL2) |
MDD | major depressive disorder |
mesLN | mesenteric lymph nodes |
mesLNC | mesenteric lymph node cells |
MHC | major histocompatibility complex |
M. kyogaense | Mycobacterium kyogaense |
M. vaccae | Mycobacterium vaccae |
MyD88 | MYD88 innate immune signal transduction adaptor |
NCIB | National Collection of Industrial Bacteria |
NCTC | National Collection of Type Cultures, Central Public Laboratory Service, London, UK |
NF-κB | nuclear factor-κB |
NK | natural killer cell |
NKG2D | natural killer group 2D |
NLR | nucleotide-binding oligomerization domain (NOD)-like receptors |
NOD | nucleotide-binding oligomerization domain |
OVA | ovalbumin |
PASI | Psoriasis Area Severity Index |
PBMC | peripheral blood mononuclear cells |
PBS | phosphate-buffered saline |
PEA | palmitoylethanolamide |
PMG | proteose peptone-meat extract-glycerol agar |
p.o. | per os (i.e., orally) |
PPARα | peroxisome proliferator-activated receptor alpha |
PRR | pattern recognition receptor |
PTSD | posttraumatic stress disorder |
RA | retinoic acid |
RGMs | rapidly growing mycobacteria |
SARS-CoV-2 | severe acute respiratory syndrome coronavirus type 2 |
s.c. | subcutaneous |
SHC | single-housed control |
SN | Australian Mycological Panel |
SPF | specific pathogen-free |
TB | tuberculosis |
TCR | T cell receptor |
TGFβ1 | transforming growth factor beta 1 |
Th | T helper cell |
TLR | Toll-like receptor |
TMC | Trudeau Mycobacterial Culture Collection |
TNF | tumor necrosis factor, also referred to as tumor necrosis factor alpha |
Treg | regulatory T cells |
Veh | vehicle |
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Reference Strain | Original Source and Year of Isolation | Alternative Collection Numbers | Culture Medium | Batch Name | Inactivation Method | Administration Vehicle | Reference |
---|---|---|---|---|---|---|---|
Mycobacterium vaccae NCTC 11659 [34] | Mud (lake Kyoga, Uganda), 1973 | - DSM 107316 - CECT 9646 | - Peptone meat extract glycerol agar - Middlebrook medium - Löwenstein-Jensen medium - Tryptic Soy Agar - MB7H10 agar - PMG agar - GYM agar | SRP 299 | Heat-killed 2 | PBS | [36,37,38] |
Saline | [39,40] | ||||||
SRL172 | Heat-killed 2 | BBS | [41] | ||||
Irradiation-killed 3,* | BBS | [42] | |||||
V7 | Hydrolyzed and heat-killed 2 | Oral pill excipients | [43,44] | ||||
Dar-901 (SRL 172) | Heat-killed 2 | Citrate buffer | [45] | ||||
MV07 | Heat-killed 2 | Culture media | [46] | ||||
MV001 | Heat-killed 2 | BBS * | [47] | ||||
MV007 | Heat-killed 2 | BBS | [48] | ||||
ENG1 | Heat-killed 2 | BBS | [20,22,24,29,32] | ||||
R877R | Irradiation-killed 3 | BBS | [49] | ||||
Mycobacterium vaccae ATCC 15483T [50] | Bovine milk, 1964 | - ATCC 23004 - CCUG 21003T - DSM 43292 - KCTC 19087 - NCIB 9937 - NCTC 10916 - SN 920 (Bonicke SN920) - TMC 1526 | - Middlebrook medium - Medium 55 for Mycobacterium | V7 | Hydrolyzed and heat-killed 2 | Oral pill excipients | [51] |
M. vaccaeTM | Heat-killed 2 | Distilled water | [52] | ||||
ATCC® 15483 | Heat-killed 2 | PBS | [53] | ||||
BBS | [29] |
Disease Investigated | M. vaccae Strain | Dosage | Vehicle | Effects | Underlying Mechanisms | Reference |
---|---|---|---|---|---|---|
Tuberculosis | NCTC 11659 | 1 dose (i.d.; 1 mg in 0.1 mL) | BBS | - improved clearance of TB bacilli - normalized ESR - improved sputum conversion - increased survival | - reduced serum IL-4, IL-10, TNF - increased serum IFNγ | [54,55,56,57] |
Tuberculosis | NCTC 11659 (SRL172) | 3 doses (i.d.; 1 mg in 0.1 mL) | BBS | - improved clearance of TB bacilli - normalized ESR - improved sputum conversion | increased serum IL-4 & TNF | [41] |
Tuberculosis | NCTC 11659 (SRL172) | 10 doses (p.o; day 0,7,14,21,28 and then monthly; 1 mg/dose) | Gelatine tablet | - normalized ESR - improved sputum conversion and body weight gain | - increased Th1 parameters - decreased Th2 parameters | [58] |
Tuberculosis | NCTC 11659 (SRL172) | 5 doses (i.d.; 1 mg in 0.1 mL) | BBS | proliferation of PBMCs | increased IFNγ in PBMCs | [42] |
Tuberculosis | NCTC 11659 (V7) | 30 doses (p.o.; 10 μg/tablet) | V7 tablet (Immunitor®) | improved clearance of TB bacilli | -reduced blood leukocyte number | [43,44] |
Tuberculosis | Longcom batch (ATCC 15483T) | 30 doses (p.o.; 10 μg/tablet) | V7 tablet (Immunitor®) | improved clearance of TB bacilli | not investigated | [51] |
Leprosy | NCTC 11659 | 1 dose (i.d.; 0.1 mg in 0.1 mL) | BBS | positive Leprosin A response | not investigated | [59,60] |
Leprosy | NCTC 11659 | 1 dose (i.d.; 1 mg in 0.1 mL) | BBS | improved skin capillary flow | not investigated | [61] |
Leprosy | NCTC 11659 | 3 doses (i.d.; 0.01, 0.1, 1 mg in 0.1 mL) | BBS | positive Leprosin A response | not investigated | [62] |
Psoriasis | NCTC 11659 | 1 dose (i.d.; 1 mg in 0.1 mL) | BBS | reduced PASI | reduced lymphocyte proliferation | [63] |
Dermatitis | NCTC 11659 (SRL172) | 1 dose (i.d.; 3 mg in 0.3 mL) | BBS | reduced dermatitis lesion area | not investigated | [64] |
Asthma | NCTC 11659 (SRL172) | 1 dose (i.d.; 1 mg in 0.1 mL) | BBS | trend towards improved airway response to allergen | reduced IL-5 and IgE in PBMCs | [65] |
Cancer 2 | NCTC 11659 (SRL172) | - 1 dose (i.d.; 0.5 mg in 0.1 mL); - 3 doses (i.d.; 1 mg in 0.1 mL) | BBS | increased survival | not investigated | [66] |
Cancer 2 | NCTC 11659 (SRL172) | - 1 dose (i.d.; 50 µL (5 × 108 heat-killed bacilli)); - 4 doses (i.d.; 100 µL (109 heat-killed bacilli)) | BBS | improved survival | intracellular IL-2 induction | [67] |
Cancer 3 | NCTC 11659 (SRL172) | 5 doses (i.d.; 1 mg in 0.1 mL) | BBS | - improved quality of life (cognitive function and vitality); - reduced body pain, nausea and dyspnea | not investigated | [68] |
Disease Investigated | M. vaccae Strain | Dosage | Vehicle | Effects | Underlying Mechanisms | Reference |
---|---|---|---|---|---|---|
Negative consequences of stress | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | reduced stress-induced anxiety and colitis | - increased number of Treg (CD4+ CD25+ FoxP3+) - increased IL-10 | [20,33] |
Negative consequences of stress | NCTC 11659 | 3 doses (i.n.; 0.1 mg in 0.012 mL) | BBS | reduced stress-induced colitis | not investigated | [32] |
Negative consequences of stress | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | enhanced between- and within-session extinction in fear-potentiated startle paradigm | alteration in serotonergic gene expression | [25,27,28] |
Negative consequences of stress | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | prevention of stress-induced exaggeration of anxiety and microglial priming | - upregulated hippocampal IL4, Cd200r1 and Mrc1 - downregulated hippocampal Nlrp3 and Nfkbia | [24] |
Negative consequences of stress | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | prevention of post-operative cognitive dysfunction | - upregulated hippocampal IL4, Arg1 and Foxp3 - downregulated hippocampal NfκBbia and IL1β | [22] |
Negative consequences of stress | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | prevention of negative outcomes of a two-hit stress models | - prevention of stress-induced decreased Tph2 and Slc6a4 expression - prevention of stress-induced REM sleep disturbances | [23,26] |
Cellular/ Molecular Target Investigated | M. vaccae Strain | Dosage | Vehicle | Species | Underlying Mechanisms | Reference |
---|---|---|---|---|---|---|
Th1/Th2 balance | NCTC 11659 (MV07) | 1, 10, 100 µg/mL (in vitro) | BBS | human (DCs) | - reduced IL-4 - upregulated CD83 and CD86 | [46] |
Th1/Th2 balance | NCTC 11659 (SRL172) | 3 doses (s.c.; 106,107,108 bacteria in 0.1 mL) | BBS | mouse | - reduced serum IgE, IL-4 and IL-5 - reduced eosinophil count in BAL | [69] |
Th1/Th2 balance | NCTC 11659 | 1 dose (s.c.; 107, 108 or 109 bacteria in 0.1 mL) | BBS | mouse | - reduced serum IgE and IL-4 - increased IL-2 in splenocytes | [70] |
γδ T cells | NCTC 11659 (SRL172) | 100 μg/mL (in vitro) | BBS | human (PBMCs) | upregulated IFNγ, TNF and granzyme B | [71] |
CD11b+ myeloid cells | NCTC 11659 | 300 μg/mL (in vitro) | BBS | human (PBMCs) | - downregulated CD62L - upregulated TLR2, TLR4, CD18, CD11a, CD14, CD36, CD44, CD45, CD54 CD58k, CD80, CD86, CD137L, CD206 | [72] |
CD11c+ APC | NCTC 11659 (SRP299) | 1 dose (s.c.; 0.1 mg in 0.1 mL) | NaCl | mouse | - decreased cell number in BAL; - increased IL-10+ and TGFβ in lung DCs | [39] |
CD14+ monocytes | ATCC 15483T (SN920) | in vitro incubation with 1:10 ratio cells:mycobacteria | Medium | human (PBMCs) | increased secretion of TNF and IL-12 | [73] |
CD8+ CTL | ATCC 15483T | 1 dose (i.p.; 1 mg in 0.1 mL) | PBS | mouse | - increased expression of IFNγ in TB-infected macrophages - increased cytotoxic activity of CTL against TB-infected macrophages | [74] |
Tregs | NCTC 11659 (SRP299) | 1 dose (s.c.; 0.1 mg in 0.2 mL) | NaCl | mouse | - increased number of Treg (CD4+ CD45RBLo) - suppressed airway inflammation upon Treg transfer | [40] |
Tregs | NCTC 11659 (SRP299) | - 1 dose (i.g.; 0.1 mg in 0.1 mL) - 100, 200 or 400 μg/mL (in vitro) | -H2O-NaCl | mouse | - reduced cellular infiltrate in lungs - increased IL-10 in mesLNC | [75] |
Tregs | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | mouse | - increased number of Treg (CD4+ CD25+ FoxP3+) - increased IL-10 - reduced stress-induced anxiety and colitis | [33] |
PPARα | 10(Z)-HDA from NCTC 11659 | 200 µM (in vitro) | DMEM/F-12 | mouse | PPARα-dependent downregulation of pro-inflammatory transcription factors, cytokines and chemokines | [76] |
Serotonergic neurons | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | mouse | activation of serotonergic neurons in interfascicular part of dorsal raphe nucleus | [21] |
Microglia | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | rat | - increased expression of Il4 mRNA and IL-4-responsive genes (Cd200r1, Mrc1) - reduced IL-1β secretion from freshly isolated and LPS-stimulated hippocampal microglia | [24] |
Microglia | NCTC 11659, ATCC 15483T | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | rat | prevention of stress-induced upregulation of hippocampal Il6 mRNA expression | [29] |
Microglia | NCTC 11659 | 3 doses (s.c.; 0.1 mg in 0.1 mL) | BBS | rat | increased hippocampal Il4, Foxp3, Arg1, decreased Il1β, Il6 and Nfκbia mRNA expression | [22] |
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Amoroso, M.; Langgartner, D.; Lowry, C.A.; Reber, S.O. Rapidly Growing Mycobacterium Species: The Long and Winding Road from Tuberculosis Vaccines to Potent Stress-Resilience Agents. Int. J. Mol. Sci. 2021, 22, 12938. https://doi.org/10.3390/ijms222312938
Amoroso M, Langgartner D, Lowry CA, Reber SO. Rapidly Growing Mycobacterium Species: The Long and Winding Road from Tuberculosis Vaccines to Potent Stress-Resilience Agents. International Journal of Molecular Sciences. 2021; 22(23):12938. https://doi.org/10.3390/ijms222312938
Chicago/Turabian StyleAmoroso, Mattia, Dominik Langgartner, Christopher A. Lowry, and Stefan O. Reber. 2021. "Rapidly Growing Mycobacterium Species: The Long and Winding Road from Tuberculosis Vaccines to Potent Stress-Resilience Agents" International Journal of Molecular Sciences 22, no. 23: 12938. https://doi.org/10.3390/ijms222312938