Clinical significance of milk gangliosides in the regulation of brain and bowel functions in children

Abstract

Gangliosides are glycosphingolipids that widespread in all tissues and fluids of mammals and humans. They mainly found in ganglion cells of nervous tissue and were named from this issue. Gangliosides important components of plasma membranes and significantly contribute the growth, differentiation of neural networks, immune protection, the formation of a healthy microbiota, the prevention of metabolic disorders (such as obesity, insulin-resistant conditions) and malignant neoplasms. Gangliosides play a significant role in periods of the most active growth and differentiation of body tissues. Breast milk is the main source of gangliosides after birth. They concentrated on the membrane of the milk fat globule. The use of breast milk in the diet of children and milk formula enriched with concentrated membranes of fat globules allow modulating physiological processes during the early development of the child. We speculate that gangliosides can program the health of newborns for the future.

Keywords:breast milk, milk fat globule membrane, gangliosides, cerebroside, ceramides, phospholipids, sphingomyelin, neurogenesis, synaptogenesis, cognitive function, microbiota, neural networks, enterotoxin, cerebral palsy, metabolic disorders, obesity, enterocyte membranes, cell-cell recognition, infection, immunity, inflammation

For citation: Fedorova L.A. Clinical significance of milk gangliosides in the regulation of brain and bowel functions in children. Neonatologiya: novosti, mneniya, obuchenie [Neonatology: News, Opinions, Training]. 2019; 7 (4): 35-44. doi: 10.24411/2308-2402-2019-14004 (in Russian)

References

1. Zhdankin A.E., Ushakova G.A Structural and functional characteristic of ganglioside. Molodij vchenij [Young Scientist]. 2014; 11 (14): 258-62. (in Russian)

2. Schnaar R.L., Gerardy-Schahn R. Sialic acid in the brain: Gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev. 2014; 94 (2): 461-518.

3. Krepe E.M. Lipids of cell membranes. Leningrad: Nauka; 1981: 339 p. (in Russian)

4. Avrova N.F., Karpova O.B., Nalyvayeva N.N. Content and composition of gangliosides from nervous of a sea urchin strongl yocentrotus interme-dius. Journal of Evolutionary Biochemistry and Physiology. 1983; 19: 127.

5. McDaniel R., McLaughlin S. The interaction of calcium with gangliosides in bilayer membranes. Biochem Biophys Acta. 1985; 819 (2): 153-60.

6. Ledeen, R.W. Nuclear sphingolipids: Metabolism and signaling. Lipid Res. 2008; 49: 1176-86.

7. Nowycky M.C., Wu G., Ledeen R.W. Glycobiology of ion transport in the nervous system. Adv Neurobiol. 2014; Vol. 9: 321-42.

8. Mahadic S.P., Hawver D.B., Hangung B.K., et al. GM1 ganglioside treatment after global ischemia protects changes in membrane fatty acids. In: Calne D.B. (ed) Neurodegenerative deseases. Philadelph, Saunders, Harcourt, Brace and World. 1994; 277-99.

9. Toffano G.E. Savoini G., Moroni F., et al. Chronic GM1 ganglioside treatment reduces dopamine cell body degeneration in the substantia nigra after unilateral hemitransection in rat. Brain Res. 1984; 256 (2): 233-9.

10. Polak J.M., Bloom S.R. The diffuse neuroendocrine system. Studies of this newly discovered controlling system in health and disease. J Histochem Cytochem. 1979; 27 (10): 1398-400.

11. Tumanova S.Yu., Prokhorova M.I. Participation of gangliosides in neuronal membrane modification. Nejrohimija [Neurochemistry]. 1982; 1 (2): 184-99. (in Russian)

12. Glebov R.P., Kryzhanovskij G.N. Functional biochemistry of synapses. Moscow: Meditsina, 1978: 323 p. (in Russian)

13. Svennerholm L. Biological significance of gangliosides. In: Cellular and pathological aspects of glycoconjugate metabolism. Eds by H. Dreyfus, et al. Paris: Inserm, 1984: 21-44.

14. Wang B., Brand-Miller J. The role and potential of sialic acid in human nutrition. Eur J Clin Nutr. 2003; 57: 1351-69.

15. McJarrow P., Schnell N., Jumpsen J. Influence of dietary ganglio-sides on neonatal brain development Clandinin. Nutrition Reviews. 2009; 67 (8):451-63.

16. Mavlikhanova A.A., Pavlov V.N., Yang B., Kataev V.A., et al. Gangliosides and their significance in the development and functioning of the nervous system. Medicinskij vestnik Bashkortostana [Bashkortostan Medical Journal]. 2017; 12 (4): 121-6. (in Russian)

17. Svennerholm L., Bostrom K., Fredman P., Mansson J.E., et al. Human brain gangliosides: developmental changes from early fetal stage to advanced age. Biochim Biophys Acta. 1989; 1005 (2): 109-17.

18. Segler-Stahl K., Webster J.C., Brunngraber E.G. Changes in the concentration and composition of human brain gangliosides with aging. Gerontology. 1983; 29: 161-8.

19. Svennerholm L. Chromatographic separation of human brain gan-gliosides. J Neurochem. 1963; 10: 613-23.

20. Rueda R. The role of dietary gangliosides on immunity and the prevention of Infection. Br J Nutr. 2007; 98 (1): 68-73.

21. Park E.J., Suh M., Ramanujam K., Steiner K., et al. Diet-induced changes in membrane gangliosides in rat intestinal mucosa, plasma and brain. J Pediatr Gastroenterol Nutr. 2005; 40: 487-95.

22. Ruhl A. Glial cells in the gut. Neurogastroenterol Motil. 2005; 17: 777-90.

23. Wang J., Cheng A. Ganglioside GD3 is required for neurogenesis and long-term maintenance of neural stem cells in the postnatal mouse brain. J Neurosci. 2014; 34: 13790-800.

24. Tajima 0. Reduced motor and sensory functions and emotional response in GM3-only mice: Emergence from early stage of life and exacerbation with aging. Behav Brain Res. 2009; 198: 74-82.

25. Simpson M.A. Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat Genet. 2004; 36: 1225-9.

26. Schneider J.S., Gollomp S.M., Sendek S., Colcher A., et al. A randomized, controlled, delayed start trial of GM1 ganglioside in treated Parkinson’s disease patients. J Neurol Sci. 2013; 324: 140-8.

27. Geisler F.H., Coleman W.P., Grieco G., Poonian D. The Sygen multicenter acute spinal cord injury study. Spine. 2001; 26: 87-98.

28. Xi Ai-ping, Xu Zhong-xin, Liu Feng-li, Xu Yan-li. Neuroprotective effects of monosialotetrahexosylganglioside. Neural Regen Res. 2015; 10: 1343-4.

29. Van Heyningen W.E., Miller P.A. The fixation of tetanus toxin by ganglioside. J Gen Microbiol. 1961; 24: 107-19.

30. Swaminathan S. Molecular structures and functional relationships in clostridial neurotoxins. J. FEBS. 2011; 278: 4467-85.

31. Benson M.A., Fu Z., Kim J.J., Baldwin M.R. Unique ganglioside recognition strategies for clostridial neurotoxins. J Biol Chem. 2011; 286: 34015-22.

32. Connell T.D. Cholera toxin, LT-I, LT-IIa and LT-IIb: the critical role of ganglioside binding in immunomodulation by type I and type II heat-labile enterotoxins. Expert Rev Vaccines 6. 2007: 821-34.

33. Fukuta S., Magnani J.L., Twiddy E.M., Holmes R.K., et al. Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect Immun. 1988; 56: 1748-53.

34. Efremenko V.I., Narbutovich N.I., Khodova N.F. et al. Gangliosids -receptors of bacterial toxins and other biologically active agents. In: The annotated bibliographic index of russian and foreign literature 1976-1986. Volgograd, 1988; 202. (in Russian)

35. Tanabe A., Matsuda M., Fukuhara A., Miyata Y., et al.Obesity causes a shift in metabolic flow of gangliosides in adipose tissues. Biochem Biophys Res Commun. 2009; 379: 547-52.

36. Coleman R.A. The role of placenta in lipid metabolism. Seminars Perinatol. 1989; 13: 180-91.

37. Das T., Sa G., Mukherjea M. Characterization of cardiac fatty acidbinding protein from human placenta. Comparison with placenta heaptic types. Eur J Biochem. 1993; 211: 725-30.

38. Gustavsson M., Hodgkinson S.C., Fong B., Norris C., et al. Maternal supplementation with a complex milk lipid mixture during pregnancy and lactation alters neonatal brain lipid composition but lacks effect on cognitive function in rats. Nutr Rew. 2010; 30: 279-89.

39. Ukraintsev S.E., McJarrow P. Food and development of a brain: modern representations and prospection. Pediatrija [Pediatrics]. 2012; 91 (1): 101-7. (in Russian)

40. Fedorova L.A. Clinical significance of milk fat globule membranes in the nutrition of newborns and infants. Neonatologiya: novosti, mneniyz, obuchenie [Neonatology: News, Opinions, Training]. 2018; 6 (4): 49-57. (in Russian)

41. Ando S. Gangliosides in the nervous system. Neurochem Int. 1983; 5: P. 507-37.

42. Rueda R, Gil A. Role of gangliosides in infant nutrition. In: Huang Y.-S., Sinclair A.J. Lipids in infant nutrition. 1998. Champaign, IL, A0CS Press: 213-34.

43. Vainer M.T., et al. Developmental profiles of gangliosides in human and brain. J Neurochem. 1971. Vol.18. P. 581-592.

44. Rueda R, Tabsh K, Ladisch S. Detection of complex gangliosides in human amniotic fluid. FEBS Lett. 1993; 328: 13-6.

45. Li R., Ladisch S. Shedding of human neuroblastoma gangliosides. Biomed Biochim Acta. 1991; 1083: 57-64.

46. Laegreid A., Otnaess A.B.K. Trace amounts of ganglioside GM1 in human milk inhibits enterotoxin from Vibrio cholerae and Escherichia coli. Life Sci.1987; 40: 55-62.

47. Rueda R., Maldonaldo J., Narbona E., Gil A. Neonatal dietarygan-gliosides. Early Hum Dev. 1998; 53 (Suppl): 135-47.

48. Teneberg S., Willemsen P., de Graaf F.K., Karlsson K.A. Calf small intestine receptors for K99 fimbriated enterotoxigenic Escherichia coli. FEMS Microbiol Lett. 1993; 109: 107-12.

49. Idota T., Kawakami H., Nakajima I. Growth-promoting effects of N-acetylneuraminic acid-containing substances on bifidobacteria. Biosci Biotech Biochem. 1994; 58: 1720-2.

50. Schnabl K.L., Larcelet M., Thomson A.B., Clandinin M.T. Uptake and fate of ganglioside GD3 in human intestinal Caco-2 cells. Am J Physiol Gastrointest Liver Physiol. 2009; 297: 52-9.

51. Schnabl K.L., Larsen B., Van Aerde J.E., Lees G., et al. Gangliosides protect bowel in an infant model of necrotizing enterocolitis by suppressing proinflammatory signals. J Pediatr Gastroenterol Nutr. 2009; 49: 382-92.

52. Miklavcic J.J., Schnabl K.L., Mazurak V.C., Thomson A.B., et al. Dietary ganglioside reduces proinflammatory signalling in the intestine. J Nutr Metabol. 2012; 2012: 280-6.

53. Yuasa H., Scheinberg D.A., Houghton A.N. Gangliosides of T lymphocytes: evidence for a role in T-cell activation. Tissue Antigens. 1990; 36: 47-56.

54. Nakamura K., Suzuki H., Hirabayashi Y., Suzuki A. IV alpha (NeuGc alpha 2-8NeuGc)-Gg4Cer is restricted to CD4+ T cells producing interleukin-2 and a small population of mature thymocytes in mice. J Biol Chem. 1995; 270: 3876-81.

55. Ebel F., Scmitt E., Peter-Katalinic J., Kniep B., et al. Gangliosides: differentiation markers for murine T helper lymphocyte subpopulations TH1 and TH2. Biochemistry. 1992; 31: 12190-7.

56. Lopez P.H., Schnaar R.L. Gangliosides in cell recognition and membrane protein regulation. Curr Opin Struct Biol. 2009; 19: 549-57.

57. Palmano K., Rowan A., Guillermo R., Guan J., McJarrow P. The role of gangliosides in neurodevelopment. Nutrients. 2015; 7: 3891-913.

58. Gurnida D.A., Rowan A.M., Idjradinata P., Muchtadi D., et al. Association of complex lipids containing gangliosides with cognitive development of 6-month-old infants. /Early Human Development. 2012; 88 (8): 595-601.

59. Wang B., McVeagh P., Petocz P., Brand-Miller J. Brain gangliosides and glycoprotein sialic acid in breastfed compared with formula-fed infants. Am J Clin Nutr. 2003; 78: 1024-9.

60. Xu X-Z, Zhu T-C. Effect of ganglioside in repairing the neurological function of children with cerebral palsy: analysis of the curative efficacy in 2230 cases. Chin J Clin Rehab. 2005; 9: 122-3 (in Chinese)

All articles in our journal are distributed under the Creative Commons Attribution 4.0 International License (CC BY 4.0 license)

CHIEF EDITOR
CHIEF EDITOR
Degtyarev Dmitriy Nikolaevich
Doctor of Medical Sciences, Professor, Deputy Director for Scientific Research of the V.I. Kulakov Obstetrics, Gynecology and Perinatology National Medical Research Center of Ministry of Healthсаre of the Russian Federation, Head of the Chair of Neonatology at the Clinical Institute of Children's Health named after N.F. Filatov, I.M. Sechenov First Moscow State Medical University, Chairman of the Ethics Committee of the Russian Society of Neonatologists, Moscow, Russian Federation

ORCID iD 0000-0001-8975-2425

Journals of «GEOTAR-Media»