Home Fermented maize slurry (Ogi) and its supernatant (Omidun) mitigate elevated intraocular pressure by modulating BDNF expression and glial plasticity in the retina-gut axis of glaucomatous rats
Article
Licensed
Unlicensed Requires Authentication

Fermented maize slurry (Ogi) and its supernatant (Omidun) mitigate elevated intraocular pressure by modulating BDNF expression and glial plasticity in the retina-gut axis of glaucomatous rats

  • Adedamola Adediran Fafure EMAIL logo , Edem Ekpenyong Edem , Abiola Oluwatosin Obisesan , Linus Anderson Enye , Adeshina Oloruntoba Adekeye , Adedeji Enitan Adetunji , Kate Eberechukwu Nebo , Adebayo Adeoluwa Olusegun and Oluwabukola Eniola Fafure
Published/Copyright: August 10, 2021

Abstract

Objectives

Growing interest has been reported on the health benefits of fermented foods, which includes cognition enhancement and inflammation attenuation. BDNF is a known protectant against retinal degeneration, however, therapies that target this neurotrophic factor has been limited. Therefore, we assessed the reaction of BDNF and glial cells in glaucomatous rats and their response to treatment with fermented maize products.

Methods

Thirty male adult rats were either injected via the episcleral vein with hypertonic saline to elevate intraocular pressure (IOP) or treated with fermented maize slurry (Ogi) or its supernatant (Omidun). Following sacrifice, the retina and duodenum were studied by immunohistochemical analysis using antibodies directed against GFAP, AIF-1 and BDNF.

Results

Hypertonic saline injection produced hypertrophy of the Müller cells and increased GFAP and AIF-1 expression in the retina and gut when compared to the control. Treatment with Ogi and Omidun produced varying degrees of reduction of gliosis, protection against hypertonic saline-induced retinal ganglion cell loss, and reduced intraocular pressure. BDNF expression was downregulated following the hypertonic saline assault, while Omidun and Ogi treatment abrogated its reduction following the hypertonic saline assault.

Conclusions

Collectively, our findings suggest that acute elevation of IOP alters crosstalk between gut and retina with consequent aberrant activation of glial cells; and that probiotic bacteria like the lactic acid bacteria rich in fermented foods including Ogi and Omidun may offer neuroprotection to the ganglionic cells by attenuating the retinal glial reaction and improving BDNF activity.


Corresponding author: Adedamola Adediran Fafure, Neuroscience Unit, Department of Anatomy, Faculty of Basic Medical Sciences, College of Medicine and Health Sciences, Afe Babalola University, Ado-Ekiti, Nigeria, E-mail: , Phone: +2348069501996.

  1. Research funding: None declared.

  2. Author contribution: FAA: Original draft, investigation, conceptualization, methodology. EEE: Original draft, writing - review and editing. OAO: Methodology, Viability study and LAB count. FOE: Statistical analysis. ELA: writing - review and editing, resources. AAE: writing - review and editing. AAO: review and editing. NKE: review and editing.

  3. Conflict of interest: The authors declare no conflict of interest.

  4. Informed consent: Informed consent was obtained from all individuals included in this study.

  5. Ethical approval: This study was approved by the Animal Ethics Committee of Afe Babalola University (AB/EC/19/02/197).

References

1. Liu, S. Neurotrophic factors in enteric physiology and pathophysiology. Neuro Gastroenterol Motil 2018;30:1–13. https://doi.org/10.1111/nmo.13446.Search in Google Scholar PubMed PubMed Central

2. Liang, Y, Yu, YH, Yu, HJ, Ma, LS. Effect of BDNF-TrKB pathway on apoptosis of retinal ganglion cells in glaucomatous animal model. Eur Rev Med Pharmacol Sci 2019;23:3561–8. https://doi.org/10.26355/eurrev_201905_17777.Search in Google Scholar PubMed

3. Eastlake, K, Luis, J, Limb, GA. Potential of Müller Glia for retina neuroprotection. Curr Eye Res 2020;45:339–48. https://doi.org/10.1080/02713683.2019.1648831.Search in Google Scholar PubMed

4. Reichenbach, A, Bringmann, A. Glia of the human retina. Glia 2020;68:768–96. https://doi.org/10.1002/glia.23727.Search in Google Scholar PubMed

5. Gao, H, L, A, Huang, X, Chen, X, Xu, H. Müller Glia-mediated retinal regeneration. Mol Neurobiol 2021;58:2342–61. https://doi.org/10.1007/s12035-020-02274-w.Search in Google Scholar PubMed

6. Campbell, LJ, Hobgood, JS, Jia, M, Boyd, P, Hipp, RI, Hyde, DR. Notch3 and DeltaB maintain Müller glia quiescence and act as negative regulators of regeneration in the light-damaged zebrafish retina. Glia 2021;69:546–66. https://doi.org/10.1002/glia.23912.Search in Google Scholar PubMed

7. Guimarães RP de, M, Landeira, BS, Coelho, DM, Golbert, DCF, Silveira, MS, Linden, R, et al.. Evidence of müller glia conversion into retina ganglion cells using neurogenin2. Front Cell Neurosci 2018;12:410. https://doi.org/10.3389/fncel.2018.00410.Search in Google Scholar PubMed PubMed Central

8. Telegina, DV, Kolosova, NG, Kozhevnikova, OS. Immunohistochemical localization of NGF, BDNF, and their receptors in a normal and AMD-like rat retina. BMC Med Genom 2019;12(2 Suppl). https://doi.org/10.1186/s12920-019-0493-8.Search in Google Scholar PubMed PubMed Central

9. Johnson, EC, Guo, Y, Cepurna, WO, Morrison, JC. Neurotrophin roles in retinal ganglion cell survival: lessons from rat glaucoma models. Exp Eye Res 2009;88:808–15. https://doi.org/10.1016/j.exer.2009.02.004.Search in Google Scholar PubMed PubMed Central

10. Minckler, DS, Bunt, AH. Axoplasmic transport in ocular hypotony and papilledema in the monkey. Arch Ophthalmol 1977;95:1430–6. https://doi.org/10.1001/archopht.1977.04450080140018.Search in Google Scholar PubMed

11. Levy, NS. The effect of elevated intraocular pressure on axoplasmic transport in the optic nerve of the rhesus monkey. Doc Ophthalmol 1977;43:181–216. https://doi.org/10.1007/bf01569197.Search in Google Scholar

12. Martin, KRG, Quigley, HA, Valenta, D, Kielczewski, J, Pease, ME. Optic nerve dynein motor protein distribution changes with intraocular pressure elevation in a rat model of glaucoma. Exp Eye Res 2006;83:255–62. https://doi.org/10.1016/j.exer.2005.11.025.Search in Google Scholar PubMed

13. Quigley, HA. Ganglion cell death in glaucoma: pathology recapitulates ontogeny. Aust N Z J Ophthalmol 1995;23:85–91. https://doi.org/10.1111/j.1442-9071.1995.tb00135.x.Search in Google Scholar PubMed

14. Iwabe, S, Moreno-Mendoza, NA, Trigo-Tavera, F, Crowder, C, García-Sánchez, GA. Retrograde axonal transport obstruction of brain-derived neurotrophic factor (BDNF) and its TrkB receptor in the retina and optic nerve of American Cocker Spaniel dogs with spontaneous glaucoma. Vet Ophthalmol 2007;10(1 Suppl):12–9. https://doi.org/10.1111/j.1463-5224.2007.00504.x.Search in Google Scholar PubMed

15. Vrabec, JP, Levin, LA. The neurobiology of cell death in glaucoma. Eye 2007;21:S11–4. https://doi.org/10.1038/sj.eye.6702880.Search in Google Scholar PubMed

16. Vecino, E, García-Grespo, D, García, M, Martinez-Millán, L, Sharma, SC, Carrascal, E. Rat retinal ganglion cells co-express brain derived neurotrophic factor (BDNF) and its receptor TrkB. Vis Res 2002;42:151–7. https://doi.org/10.1016/s0042-6989(01)00251-6.Search in Google Scholar PubMed

17. Chaiwiang, N, Poyomtip, T. Microbial dysbiosis and microbiota–gut–retina axis: the lesson from brain neurodegenerative diseases to primary open-angle glaucoma pathogenesis of autoimmunity. Acta Microbiol Immunol Hung 2019;66:541–58. https://doi.org/10.1556/030.66.2019.038.Search in Google Scholar PubMed

18. Quigley, H, Broman, AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol 2006;90:262–7. https://doi.org/10.1136/bjo.2005.081224.Search in Google Scholar PubMed PubMed Central

19. Broadway, DC, Grierson, I, O’brien, C, Hitchings, RA. Adverse effects of topical antiglaucoma medication: II. The outcome of filtration surgery. Arch Ophthalmol 1994;112:1446–54. https://doi.org/10.1001/archopht.1994.01090230060021.Search in Google Scholar PubMed

20. Broadway, DC, Grierson, I, O’brien, C, Hitchings, RA. Adverse effects of topical antiglaucoma medication: I. The conjunctival cell profile. Arch Ophthalmol 1994;112:1437–45. https://doi.org/10.1001/archopht.1994.01090230051020.Search in Google Scholar PubMed

21. Schwab, I, Linberg, J, Gioia, V, Benson, W, Chao, G. Foreshortening of the inferior conjunctival fornix associated with chronic glaucoma medications. Ophthalmology 1992;99:197–202. https://doi.org/10.1016/s0161-6420(92)32001-9.Search in Google Scholar PubMed

22. Skuta, GL, Parrish, RK. Wound healing in glaucoma filtering surgery. Surv Ophthalmol 1987;32:149–70. https://doi.org/10.1016/0039-6257(87)90091-9.Search in Google Scholar PubMed

23. Rowan, S, Taylor, A. The role of microbiota in retinal disease. Adv Exp Med Biol 2018:429–35. https://doi.org/10.1007/978-3-319-75402-4_53.Search in Google Scholar PubMed

24. SaeidiFard, N, Djafarian, K, Shab-Bidar, S. Fermented foods and inflammation: a systematic review and meta-analysis of randomized controlled trials. Clin Nutr ESPEN 2020;35:30–9. https://doi.org/10.1016/j.clnesp.2019.10.010.Search in Google Scholar PubMed

25. Audu, HJ, Abiodun, OA, Ayeni, FA. Beneficial effects of a fermented maize product with its supernatant, lactobacillus fermentum and lactobacillus brevis in rat model of colitis. N Afr J Food Nutr Res 2019;03:195–200. https://doi.org/10.51745/najfnr.3.6.195-200.Search in Google Scholar

26. Kwasi, RE, Aremu, IG, Dosunmu, QO, Ayeni, FA. Viability of lactic acid bacteria in different components of Ogi with anti diarrhoeagenic E. coli activities. N Afr J Food Nutr Res 2019;03:206–13. https://doi.org/10.51745/najfnr.3.6.206-213.Search in Google Scholar

27. Edem, EE, Nathaniel, BU, Nebo, KE, Obisesan, AO, Olabiyi, AA, Akinluyi, ET, et al.. Lactobacillus plantarum mitigates sexual-reproductive deficits by modulating insulin receptor expression in the hypothalamic-pituitary-testicular axis of hyperinsulinemic mice. Drug Metab Pers Ther [Internet]. 2021 May 17. Available from: https://pubmed.ncbi.nlm.nih.gov/34002580/ [Accessed 4 Jun 2021].10.1515/dmpt-2021-1000195Search in Google Scholar PubMed

28. Gossman, CA, Linn, DM, Linn, C. Glaucoma-inducing procedure in an in vivo rat model and whole-mount retina preparation. JoVE 2016;2016:1–10. https://doi.org/10.3791/53831.https://doi.org/10.3791/53831Search in Google Scholar PubMed PubMed Central

29. Moore, CG, Epley, D, Milne, ST, Morrison, JC. Long-term non-invasive measurement of intraocular pressure in the rat eye. Curr Eye Res 1995;14:711–7. https://doi.org/10.3109/02713689508998499.Search in Google Scholar PubMed

30. Bekinschtein, P, von Bohlen und Halbach, O. Cellular and molecular mechanisms of neurotrophin function in the nervous system. Front Cell Neurosci 2020;14:101. https://doi.org/10.3389/fncel.2020.00101.Search in Google Scholar PubMed PubMed Central

31. Binley, KE, Ng, WS, Barde, Y-A, Song, B, Morgan, JE. Brain-derived neurotrophic factor prevents dendritic retraction of adult mouse retinal ganglion cells. Eur J Neurosci 2016;44:2028–39. https://doi.org/10.1111/ejn.13295.Search in Google Scholar PubMed PubMed Central

32. Harada, C, Azuchi, Y, Noro, T, Guo, X, Kimura, A, Namekata, K, et al.. TrkB signaling in retinal glia stimulates neuroprotection after optic nerve injury. Am J Pathol 2015;185:3238–47. https://doi.org/10.1016/j.ajpath.2015.08.005.Search in Google Scholar PubMed

33. Maqsood, R, Stone, TW. The Gut-brain Axis, BDNF, NMDA and CNS disorders. Neurochem Res 2016;41:2819–35. https://doi.org/10.1007/s11064-016-2039-1.Search in Google Scholar PubMed

34. Ghani, NAA, Channip, AA, Chok Hwee Hwa, P, Ja’afar, F, Yasin, HM, Usman, A. Physicochemical properties, antioxidant capacities, and metal contents of virgin coconut oil produced by wet and dry processes. Food Sci Nutr 2018;6:1298–306. https://doi.org/10.1002/fsn3.671.Search in Google Scholar PubMed PubMed Central

35. Rosenbaum, C, Schick, MA, Wollborn, J, Heider, A, Scholz, C-J, Cecil, A, et al.. Activation of Myenteric Glia during acute inflammation in vitro and in vivo. PloS One 2016;11:e0151335. https://doi.org/10.1371/journal.pone.0151335.Search in Google Scholar PubMed PubMed Central

36. Malan, L, Hamer, M, von Känel, R, van Wyk, RD, Wentzel, A, Steyn, HS, et al.. Retinal-glia ischemia and inflammation induced by chronic stress: the SABPA study. Brain Behav Immun-Health 2020;2:100027. https://doi.org/10.1016/j.bbih.2019.100027.Search in Google Scholar

37. Vidal, L, Díaz, F, Villena, A, Moreno, M, Campos, JG. Pérez de Vargas I. Reaction of Müller cells in an experimental rat model of increased intraocular pressure following timolol, latanoprost and brimonidine. Brain Res Bull 2010;82:18–24. https://doi.org/10.1016/j.brainresbull.2010.02.011.Search in Google Scholar PubMed

38. Ramirez, AI, de Hoz, R, Salobrar-Garcia, E, Salazar, JJ, Rojas, B, Ajoy, D, et al.. The role of microglia in retinal neurodegeneration: Alzheimer’s disease, Parkinson, and glaucoma. Front Aging Neurosci 2017;9:1–21. https://doi.org/10.3389/fnagi.2017.00214.Search in Google Scholar PubMed PubMed Central

39. Wang, Y, Wang, Z, Wang, Y, Li, F, Jia, J, Song, X, et al.. The gut-microglia connection: implications for central nervous system diseases. Front Immunol 2018;9:2325. https://doi.org/10.3389/fimmu.2018.02325.Search in Google Scholar PubMed PubMed Central

40. Karlstetter, M, Scholz, R, Rutar, M, Wong, WT, Provis, JM, Langmann, T. Retinal microglia: just bystander or target for therapy? Prog Retin Eye Res 2015;45:30–57. https://doi.org/10.1016/j.preteyeres.2014.11.004.Search in Google Scholar PubMed

41. Rojas, B, Gallego, BI, Ramírez, AI, Salazar, JJ, de Hoz, R, Valiente-Soriano, FJ, et al.. Microglia in mouse retina contralateral to experimental glaucoma exhibit multiple signs of activation in all retinal layers. J Neuroinflammation 2014;11:133. https://doi.org/10.1186/1742-2094-11-133.Search in Google Scholar PubMed PubMed Central

42. Yang, HE, Li, Y, Nishimura, A, Jheng, HF, Yuliana, A, Kitano-Ohue, R, et al.. Synthesized enone fatty acids resembling metabolites from gut microbiota suppress macrophage-mediated inflammation in adipocytes. Mol Nutr Food Res 2017;61. https://doi.org/10.1002/mnfr.201700064.Search in Google Scholar PubMed

43. Choritz, L, Mansouri, K, van den Bosch, J, Weigel, M, Dick, HB, Wagner, M, et al.. Telemetric measurement of intraocular pressure via an implantable pressure sensor—12-month results from the ARGOS-02 trial. Am J Ophthalmol 2020;209:187–96. https://doi.org/10.1016/j.ajo.2019.09.011.Search in Google Scholar PubMed

Received: 2021-03-13
Accepted: 2021-07-27
Published Online: 2021-08-10

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Reviews
  3. A preliminary systematic review and meta-analysis on the effects of heart rate variability biofeedback on heart rate variability and respiration of athletes
  4. The potential positive epigenetic effects of various mind-body therapies (MBTs): a narrative review
  5. The effect of Chlorella vulgaris on obesity related metabolic disorders: a systematic review of randomized controlled trials
  6. Biological and medicinal application of Cucumis sativus Linn. – review of current status with future possibilities
  7. The effect of the herbal medicine on severity of cyclic mastalgia: a systematic review and meta-analysis
  8. Research Articles
  9. Chemical compositions, antibacterial, antifungal and cytotoxic effects of Alhagi mannifera five extracts
  10. Anticonvulsive and anti-epileptogenesis effects of Echinacea purpurea root extract, an involvement of CB2 receptor
  11. Fermented maize slurry (Ogi) and its supernatant (Omidun) mitigate elevated intraocular pressure by modulating BDNF expression and glial plasticity in the retina-gut axis of glaucomatous rats
  12. Levetiracetam exposure during prenatal and postnatal period induces cognitive decline in rat offsprings, not completely prevented by Bacopa monnieri
  13. Antibiofilm action of Persea americana glycolic extract over Acinetobacter baumannii and absence of toxicity in Galleria mellonella
  14. Validation of Unani concept of Abadāl-i-Adwiya (drug substitution) by physicochemical standardization and hepatoprotective activity of Aristolochia rotunda Linn. and its substitute Curcuma Zedoaria Rosc. in albino Wistar rats
  15. Cinnamon oil as a co-chemotherapy agent through inhibition of cell migration and MMP-9 expression on 4T1 cells
  16. Assessment of biochemical changes in normal and diabetic rats treated by phenolic enriched extracts of Juglans regia L. barks
  17. Influence of Clerodendrum volubile leaf extract on doxorubicin-induced toxicity and inhibition of carbonyl reductase mediated metabolism
  18. Quantification of anacardic acid, the toxic component in raw and purified samples of Semecarpus anacardium L. by Siddha purification processes
  19. Molecular docking and molecular dynamics approach to identify potential compounds in Huperzia squarrosa for treating Alzheimer’s disease
  20. Evaluation of ethanol extracts from three species of Artocarpus as natural gastroprotective agents: in vivo and histopathological studies
  21. Attenuation of cisplatin induced myelosuppression by methanol extract of Cedrus deodara in Wistar rats
  22. Acute and sub-acute toxicity assessment of the standardized extract of Sanguisorba minor in vivo
  23. Efficacy of lettuce seed syrup on insomnia in patients with breast cancer: a pilot double blind randomized placebo controlled clinical trial
  24. The effect of aromatherapy with rose essential oil on apparent anxiety in patients with myocardial infarction
  25. Effect of Jyoti-Trataka on intraocular pressure, autonomic control, and blood glucose in diabetic patients with high-tension primary open-angle glaucoma: a randomized-controlled trial
  26. Efficacy of Ḥammām-i-yābis (dry bath) in metabolic syndrome: a single arm, open-labelled clinical trial
  27. Effect of Ḥijāma (wet cupping), Dalk (massage) and Bukhūr (medicated steam) in amelioration of Waja al-Zahr (non-specific low back pain) – an open prospective clinical trial
  28. Effect of yoga on cardiovascular functions and psychological aspects of people on public service-related work: an exploratory study
Downloaded on 13.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/jcim-2021-0114/html
Scroll to top button