Role of gut microbiota in the progression of HIV/AIDS infection


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Acquired immune deficiency syndrome is the final stage of the progression of the infection induced by HIV. Without antiretroviral therapy, the period from the infection to the death of the patient lasts for about 10 years. The gut microbiota changes were proved to be one of the most important factor in the immune activation, local and system inflammation, as well as the progression of concomitant diseases. The aim of the review is to summarize the data describing the mechanisms of the influence of microbiome changes on the inflammation, immune activation, and HIV-associated complications. The original date of own investigations is presented too. The results confirm the endogenous way of Klebsiella infecting of AIDS patients due of the translocation from the gut.

Full Text

Restricted Access

About the authors

T. I Khomyakova

Scientific Research Institute of Human Morphology

Email: tatkhom@yandex.ru

G. V Kozlovskaya

Scientific Research Institute of Human Morphology

A. D Magomedova

Scientific Research Institute of Human Morphology

N. F Chertovich

Scientific Research Institute of Human Morphology

Yu. E Kozlovsky

Scientific Research Institute of Human Morphology

Yu. G Parkhomenko

Scientific Research Institute of Human Morphology; Infection University Hospital No 2

Yu. N Khomyakov

Anti-plague Center of Federal Service on Surveillance for Consumer rights protection and human well-being

References

  1. University College London. «HIV remission achieved in second patient». ScienceDaily. ScienceDaily, 5 March 2019. <www.sciencedaily.com/releas-es/2019/03/190305153644.htm>.
  2. Li Z., David W, Purcell, J.D., Sansom S.L., Hayes D., H. Hall I. Vital signs: HIV transmission along the continuum of care-United States, 2016// MMWR Morb Mortal Wkly Rep.2019;doi: 10.15585/mmwr.mm6811e1
  3. UNAIDS. Global AIDS update 2016. 2016. http://www.unaids.org/sites/default/files/ media_asset/global-AIDS-update2016_ en.pdf.]
  4. Grant M., Larijani M. Evasion of adaptive immunity by HIV through the action of host APOBEC3G/F enzymes.// AIDS Res Ther. 2017; 14 (1): 44. https://doi.org/10.1186/ s12981-017-0173-8.
  5. Romani B., Allahbakhshi E. Underlying mechanisms of HIV-1 latency. Virus Genes. 2017; 53 (3): 329-39. https://doi. org/10.1007/s11262-017-1443-1. Epub 2017 Mar 3.
  6. Promer K., Karris M.Y. Current Treatment Options for HIV Elite Controllers: a Review Curr. Treat Options Infect. Dis. 2018; 10 (2): 302-9. https://doi.org/10.1007/s40506-018-0158-8. Epub 2018 Apr 16.
  7. Бартлетт Дж., Галлант Дж., Фам П. Клинические аспекты ВИЧ-инфекции. 2009-2010. М.: Р. Валент, 2010; 490. ISBN 978-5-93439-298-8.
  8. Шмагель К.В., Шмагель Н.Г, Черешнев В.А. Активация иммунитета при ВИЧ-инфекции. Медицинская иммунология. 2017; 19 (5): 489-504.
  9. Stecher B. The roles of inflammation, nutrient availability and the commensalmi-crobiota in enteric pathogen infection. Microbiol Spectr. 2015; 3 (3). https://doi. org/10.1128/microbiolspec.MBp-0008-2014.
  10. Tincati C., Douek D.C. , Marchetti G. Gut barrier structure, mucosal immunity and intestinal microbiota in the pathogenesis and treatment of HIV infection//AIDS Res Ther. 2016. 13: 19. https://doi.org/10.1186/ s12981-016-0103-1
  11. Brenchley J.M., Price D.A., Schacker T.W., Asher T.E., Silvestri G., Rao S., Kazzaz Z., Bornstein E., Lambotte O., Altmann D., Blazar B.R., Rodriguez B., Teixeira-Johnson L., Landay A., Martin J.N., Hecht F.M., Picker L.J., Lederman M.M., Deeks S.G., Douek D.C. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 2006; 12: 1365-71. https://doi.org/10.1038/nm1511
  12. Brenchley J.M., Douek D.C. HIV infection and the gastrointestinal immune system. Mucosal. Immunol. 2008; 1: 23-30.
  13. Kamat A., Ancuta P., Blumberg R.S., Gabuzda D. Serological markers for inflammatory bowel disease in AIDS patients with evidence of microbial translocation. PloS ONE. 2010; 5 (11): e15533. https://doi. org/10.1371/journal.pone.0015533.
  14. Epple H.J., Schneider T., Troeger H., Kunkel D., Allers K., Moos V., Amasheh M., Loddenkemper C., Fromm M., Zeitz M., Schulzke J.D. Impairment of the intestinal barrier is evident in untreated but absent in suppressively treated HIV-infected patients. Gut. 2009; 58: 220-7. https://doi. org/10.1136/gut.2008.150425. Epub 2008 Oct 20.
  15. Wang H., Kotler D.P. HIV enteropathy and aging: gastrointestinal immunity, mucosal epithelial barrier, and microbial translocation. Curr. Opin. HIV AIDS. 2014; 9(4): 309-16. https://doi.org/10.1097/ COH.0000000000000066.
  16. Sakai E., Higurashi T., Ohkubo H., Hosono K., Ueda A., Matsuhashi N., Nakajima A. Investigation of small bowel abnormalities in HIV-infected patients using capsule endoscopy. Gastroenterology Res Pract. 2017; 1932647. https://doi. org/10.1155/2017/1932647
  17. Nazli A., Chan O., Dobson-Belaire W.N., Ouellet M., Tremblay M.J., Gray-Owen S.D., Arsenault A.L., Kaushic C. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PloS Pathogens, 2010; 6: e1000852. https:// doi.org/10.1371/journal.ppat.1000852
  18. Bode H., Lenzner L., Kraemer O.H., Kroesen A.J., Bendfeldt K., Schulzke J.D., Fromm M., Stoltenburg-Didinger G., Zeitz M., Ullrich R. The HIV protease inhibitors saquinavir, ritonavir, and nelfinavir induce apoptosis and decrease barrier function in human intestinal epithelial cells. Antivir Ther. 2005; 10 (5): 645-55.
  19. Pitrak D.L., Novak R.M., Estes R., Tschampa J., Abaya C.D., Martinson J., Bradley K., Tenorio A.R., Landay A.L. Short communication: Apoptosis pathways in HIV-1-infected patients before and after highly active antiretroviral therapy: relevance to immune recovery AIDS Res Hum Retroviruses. 2015; 31 (2): 208-16. https:// doi.org/10.1089/aid.2014.0038
  20. Somsouk M., Estes J.D., Deleage C., Dunham R.M., Albright R., Inadomi J.M., Martin J.N., Deeks S.G., McCune J.M., Hunt P.W. Gut epithelial barrier and systemic inflammation during chronic HIV infection. AIDS. 2015; 29 (1): 43-51. https://doi.org/10.1097/ QAD.0000000000000511
  21. Abad-FernandezM., VallejoA., Hernandez-Novoa B., Diaz L., Gutierrez C., Madrid N., Munoz M.A., Moreno S. Correlation between different methods to measure microbial translocation and its association with immune activation in long-term suppressed HIV-1-infected individuals. J. Acquir Immune Defic Syndr. 2013; 64 (2): 149-53. https://doi. org/10.1097/QAI.0b013e31829a2f12.
  22. Estes J.D., Harris L.D., Klatt N.R., Tabb B., Pittaluga S., Paiardini M., Barclay G.R., Smedley J., Pung R., Oliveira K.M., Hirsch V.M., Silvestri G., Douek D.C., Miller C.J., Haase A.T., Lifson J., Brenchley J.M. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PloS Pathog. 2010; 6: e1001052. https://doi. org/10.1371/journal.ppat.1001052.
  23. Marchetti G., Bellistri G.M., Borghi E., Tincati C., Ferramosca S., La Francesca M., Morace G., Gori A., Monforte A.D. Microbial translocation is associated with sustained failure in CD4+ T-cell reconstitution in HIV-infected patients on longterm highly active antiretroviral therapy AIDS. 2008; 22 (15): 2035-8 https://doi. org/10.1097/QAD.0b013e3283112d29
  24. Vesterbacka J. The role of microbial translocation and gut microbiota in HIV-1 infection. Thesis The Division Of Infectious Diseases, Department Of Medicine Hud-dinge, Karolinska Institutet, Stockholm, Sweden. September 2017. https://www. researchgate.net/publication/320166500
  25. Хасанова Г.Р., Биккинина О.И., Анохин B.А. Халиуллина C.B., Яковлев М.Ю. Кишечный эндотоксин как вероятный индуктор системного воспалительного ответа при ВИЧ-инфекции. Практическая медицина. 2012; 1 (56): 52-5. [Hasanova G.R., Bikkinina O.I., Anohin V.A. Haliullina C.V., YAkovlev M.YU. Intestinal endotoxin as a likely inducer of systemic inflammatory response in HIV infection. Prakticheskaya medicina. 2012; 1 (56): 52-5 (in Russian)]
  26. Kistler J.O., Arirachakaran P., Poovorawan Y., Dahlen G.,Wade W.G. The oral micro-biome in human immunodeficiency virus (HIV)-positive individuals. J. Med. Microbiol. 2015; 64 (9): 1094-101.
  27. Berard A.R., Perner M., Mutch S., Farr Zuend C., McQueen P., Burgener A.D. Understanding mucosal and microbial functionality of the female reproductive tract by metapro-teomics: Implications for HIV transmission. Amer J. Repr. Immunol. 2018; 80 (2): 12977 https://doi.org/10.1111/aji.12977
  28. Twigg H.L. 3rd, Weinstock G.M., Knox K.S. Lung microbiome in human immunodeficiency virus infection. Transl Res. 2017; 179: 97-107. https://doi.org/10.10Wj. trsl.2016.07.008. Epub 2016 Jul 18
  29. Mamoudou S., Bellaud G., Ana C., Gilles P. Lung co-infection by Pneumocystis jirovecii and Pseudomonas aeruginosa in AIDS: report of two cases. Pan. Afr. Med. J. 2015; 21: 95. https://doi.org/10.11604/ pamj.2015.21.95.5993. eCollection 2015.
  30. Salins N., Vallath N., Prince VV Pseudomonas Bronchopulmonary Infections in a Palliative Care Setting. Indian J. Palliat Care. 2012; 18 (1): 1-5 https://doi. org/10.4103/0973-1075.97341
  31. Barantsevich N.E., Orlova O.E., Shlyakhto E.V, Johnson E.M., Woodford N., Lass-Floerl C., Churkina I.V, Mitrokhin S.D., Shkoda A.S., Barantsevich E.PEmergence of Candida auris in Russia. J. Hosp. Infect. 2019. pii: 0195-6701(19)30104-5. https://doi. org/10.1016/j.jhin.2019.02.021
  32. Sekyere J.O. Candida auris: A systematic review and meta-analysis of current updates on an emerging multidrug-resistant pathogen. Microbiologyopen. 2018; 7 (4): e00578. https://doi.org/10.1002/mbo3.578
  33. Vujkovic-Cvijin I., Dunham R.M., Iwai S., Maher M.C., Albright R.G., Broadhurst M.J., Hernandez R.D., Lederman M.M., Huang Y, Somsouk M., Deeks S.G., Hunt P.W., Lynch S.V, McCune J.M. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci Transl Med. 2013; 5, 10, 5 (193): 193ra91. https://doi.org/10.1126/ scitranslmed.3006438
  34. Mutlu E.A., Keshavarzian A., Losurdo J., Swanson G., Siewe B., Forsyth C., French A., Demarais P, Sun Y, Koenig L., Cox S., Engen P, Chakradeo P., Abbasi R., Gorenz A., Burns C., Landay A.A compositional look at the human gastrointestinal microbiome and immune activation parameters in HIV infected subjects. PLoS Pathog. 2014; 10 (2): e1003829. https://doi.org/10.1371/jour-nal.ppat.1003829.
  35. Vesterbacka J., Rivera J., Noyan K., Parera M., Neogi U., Calle M., Paredes R., Sonnerborg A., Noguera-Julian M., Nowak P Richer gut microbiota with distinct metabolic profile in HIV infected Elite Controllers Scientific Reports. 7: 6269. https://doi. org/10.1038/s41598-017-06675-1
  36. Ellis C.L., Ma Z.M., Mann S.K., Li C.S., Wu J., Knight T.H., Yotter T, Hayes T.L., Maniar A.H., Troia-Cancio PV, Overman H.A., Torok N.J., Albanese A., Rutledge J.C., Miller C.J., Pollard R.B., Asmuth D.M. Molecular characterization of stool microbiota in HIV-infected subjects by pan bacterial and order-level 16s ribosomal DNA (rDNA) quantification and correlations with immune activation. J. Acq Imm Defic Syndromes. 2011; 57 (5): 363-70. 100. https:// doi.org/10.1097/QAI.0b013e31821a603c
  37. Dillon S.M., Kibbie J., Lee E.J., Guo K., Santiago M.L., Austin G.L., Gianella S., Landay A.L., Donovan A.M., Frank D.N., McCARTER M.D., Wilson C.C. Low abundance of colonic butyrate-producing bacteria in HIV infection is associated with microbial translocation and immune activation. AIDS. 2017; 31 (4): 511-21. https://doi. org/10.1097/QAD.0000000000001366
  38. Nilsson J., Kinloch-de-Loes S., Granath A., Sonnerborg A., Goh L.E., Andersson J. Early immune activation in gut-associated and peripheral lymphoid tissue during acute HIV infection. AIDS. 2007; 21 (5): 565-74. https://doi.org/10.1097/ QAD.0b013e3280117204
  39. Pinacchio C., Scheri G.C., Statzu M., Santinelli L., Ceccarelli G., Innocenti G.P, Vullo V., Antonelli G., Brenchley J.M., d'Ettorre G., Scagnolari C. Type I/II Interferon in HIV-1-Infected Patients: Expression in Gut Mucosa and in Peripheral Blood Mononuclear Cells and Its Modification upon Probiotic Supplementation. J. Immunol Res. 2018; 2018: 1738676. https://doi. org/10.1155/2018/1738676. eCollection 2018.
  40. Gori A., Tincati C., Rizzardini G., Torti C., Quirino T., Haarman M., Amor K.B., van Schaik J., Vriesema A.,Knol J., Marchetti G., Welling G., Clerici M. Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J. Clin Microb, Feb. 2008; 46 (2): 757-8 https://doi.org/10.1128/JCM.01729-07W
  41. Neff C.P, Krueger O., Xiong K., Arif S., Nusbacher N., Schneider J.M., Cunningham A.W., Armstrong A., Li S., McCarter M.D., Campbell T.B., Lozupone C.A., Palmer B.E. Fecal Microbiota Composition Drives Immune Activation in HIV-infected Individuals. EBioMedicine. 2018; 30: 192-202. htt-ps://doi.org/10.1016/j.ebiom.2018.03.024. Epub 2018 Mar 26.
  42. Wan Saudi W.S., Sjoblom M. Short-chain fatty acids augment rat duodenal mucosal barrier function. Exp. Physiol. 2017; 102 (7): 791-803. https://doi.org/10.1113/EP086110
  43. Penny H.A., Hodge S.H., Hepworth M.R. Orchestration of intestinal homeostasis and tolerance by group 3 innate lymphoid cells. Semin Immunopathol. 2018; 40 (4): 357-70. https://doi.org/10.1007/s00281-018-0687-8. Epub 2018 May 8.
  44. Guo X., Fu YX. The tragic fate of group 3 innate lymphoid cells during HIV-1 infection. J. Clin. Invest. 2015; 125 (10): 3992. https:// doi.org/10.1172/JCI84529.
  45. Корогодская Е. Г, Умбетова К.Т, Белая О.Ф., Мазус А.И., Юдина Ю.В., Белая Ю.А., Сметанина С.В., Алленов М. Н., Пак С.Г Разнообразие ЛПС - антигенов возбудителей кишечных инфекций у больных ВИЧ-инфекцией на стадии вторичных заболеваний. Эпидемиология и инфекционные болезни. 2015; 20 (1): 4-7.
  46. Bandera A., De Benedetto I., Bozzi G., Gori A. Altered gut microbiome composition in HIV infection: causes, effects and potential intervention. Curr. Opin. HIV AIDS. 2018; 13 (1): 73-80. https://doi.org/10.1097/ COH.0000000000000429
  47. Dicks L.M., Fraser T., ten Doeschate K., van Reenen C.A. Lactic acid bacteria population in children diagnosed with human immunodeficiency virus. J. Paediatr. Child Health. 2009; 45: 567-72.
  48. Wang J., Ji H., Wang S., Liu H., Zhang W., Zhang D., Wang Y Probiotic Lactobacillus plantarum promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Front Microbiol. 2018; 9: 1953. https://doi.org/10.3389/ fmicb.2018.01953. eCollection 2018
  49. Bengmark S., Jeppsson B. Gastrointestinal surface protection and mucosa reconditioning. JPEN J. Parenter Enteral. Nutr. 1995; 19 (5): 410-5. Review.
  50. Cunningham-Rundles S., Ahrne S., Johann-Liang R., Abuav R., Dunn-Navarra A.M., Grassey C., Bengmark S., Cervia J.S. Effect of probiotic bacteria on microbial host defense, growth, and immune function in human immunodeficiency virus type-1 infection. Nutrients. 2011; 3 (12): 1042-70. https://doi.org/10.3390/nu3121042. Epub 2011 Dec 19.
  51. Kazemi A., Djafarian K., Speakman J.R., Sabour P, Soltani S., Shab-Bidar S. Effect of Probiotic Supplementation on CD4 Cell Count in HIV-Infected Patients: A Systematic Review and Meta-analysis. J. Diet Suppl. 2018; 15 (5): 776-88. https://doi.org/10.1080/ 19390211.2017.1380103. Epub 2017 Nov 29.
  52. Rijkers G.T., Bengmark S., Enck P, Haller D., Herz U., Kalliomaki M., Kudo S., Lenoir-Wijnkoop I., Mercenier A., Myllyluoma E. et al. Guidance for substantiating the evidence for beneficial effects of probiotics: Current status and recommendations for future research. J. Nutr. 2010; 140: 671-6. https://doi.org/10.3945/jn.109.113779.
  53. D'Angelo Ch., Reale M.,. Costantini E. Microbiota and Probiotics in Health and HIV Infection. Nutrients. 2017; 9 (6): 615 https:// doi.org/10.3390/nu9060615
  54. Cheng S., Ma X., Geng S., Jiang X., Li Y, Hu L., Li J., Wang Y, Han X. Fecal Microbiota Transplantation Beneficially Regulates Intestinal Mucosal Autophagy and Alleviates Gut Barrier Injury mSystems. 2018; 3 (5). pii: e00137-18. https://doi.org/10.1128/mSystems.00137-18. eCollection 2018 Sep-Oct.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies