Malnutrition in healthy individuals results in increased mixed cytokine profiles, altered neutrophil subsets and function

PLoS ONE

Volumn 11, Issue 8, 2016, Pages

  Takele, Y ^a,b   Adem, E ^b   Getahun, M ^b   Tajebe, F ^b   Kiflie, A ^b   Hailu, A ^c   Raynes, J ^d   Mengesha, B ^b   Ayele, T A ^b   Shkedy, Z ^e   Lemma, M ^b   Diro, E ^b   Toulza, F ^d   Modolell, M ^f   Munder, M ^g   Muller I ^a   Kropf, P ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF GONDAR   (Ethiopia)

^c ADDIS ABABA UNIVERSITY   (Ethiopia)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^e HASSELT UNIVERSITY   (Belgium)

^f MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^g UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; C REACTIVE PROTEIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 8; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; CYTOKINE;

ADULT; ARTICLE; BODY MASS; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DENSITY; CELL FUNCTION; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOREACTIVITY; MALE; MALNUTRITION; NEUTROPHIL; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PHYSICAL ACTIVITY; PROSPECTIVE STUDY; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; CELL LINEAGE; DISEASE PREDISPOSITION; ETHIOPIA; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MICROBIOLOGY; OPPORTUNISTIC INFECTIONS; PATHOLOGY;

ADULT; ARGINASE; BODY MASS INDEX; CD4-CD8 RATIO; CELL LINEAGE; CROSS-SECTIONAL STUDIES; CYTOKINES; DISEASE SUSCEPTIBILITY; ETHIOPIA; FEMALE; GENE EXPRESSION; HUMANS; LYMPHOCYTE ACTIVATION; MALE; MALNUTRITION; NEUTROPHILS; OPPORTUNISTIC INFECTIONS; REACTIVE OXYGEN SPECIES; TH1 CELLS;

EID: 84984981933     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0157919     Document Type: Article

References (50)

1. Bain LE, Awah PK, Geraldine N, Kindong NP, Sigal Y, Bernard N, et al. Malnutrition in Sub-Saharan Africa: burden, causes and prospects. Pan Afr Med J. 2013; 15:120. doi:10.11604/pamj.2013.15.120.2535 PMID: 24255726; PubMed Central PMCID: PMCPMC3830470.
2. Alcoba G, Kerac M, Breysse S, Salpeteur C, Galetto-Lacour A, Briend A, et al. Do children with uncomplicated severe acute malnutrition need antibiotics? A systematic review and meta-analysis. Plos One. 2013; 8(1):e53184. doi:10.1371/journal.pone.0053184 PMID: 23326395; PubMed Central PMCID: PMCPMC3541371.
3. Bhutta ZA, Salam RA. Global nutrition epidemiology and trends. Ann Nutr Metab. 2012; 61 Suppl 1:19- 27. doi: 10.1159/000345167 PMID: 23343944.
4. Rodriguez L, Cervantes E, Ortiz R. Malnutrition and gastrointestinal and respiratory infections in children: A public health problem. Int J Environ Res Public Health. 2011; 8(4):1174-205. doi:10.3390/ijerph8041174 PMID: 21695035; PubMed Central PMCID: PMCPMC3118884.
5. Shankar AH. Nutritional modulation of malaria morbidity and mortality. J Infect Dis. 2000; 182 Suppl 1: S37-S53. doi: 10.1086/315906 PMID: 10944483.
6. Schaible UE, Kaufmann SH. Malnutrition and infection: complex mechanisms and global impacts. Plos Med. 2007; 4(5):e115. doi:10.1371/journal.pmed.0040115 PMID: 17472433; PubMed Central PMCID: PMCPMC1858706.
7. Woodward B. Protein, calories, and immune defenses. Nutr Rev. 1998; 56(1 Pt2):S84-S92. PMID: 9481128.
8. Chandra RK. Nutrition and immunity in the elderly. Nutr Res Rev. 1991; 4(1):83-95. doi:10.1079/NRR19910009 PMID: 19094326.
9. Najera O, Gonzalez C, Toledo G, Lopez L, Cortes E, Betancourt M, et al. CD45RA and CD45RO isoforms in infected malnourished and infected well-nourished children. Clin Exp Immunol. 2001; 126 (3):461-5. PMID: 11737063; PubMed Central PMCID: PMCPMC1906241.
10. Rodriguez L, Gonzalez C, Flores L, Jimenez-Zamudio L, Graniel J, Ortiz R. Assessment by flow cytometry of cytokine production in malnourished children. Clin Diagn Lab Immunol. 2005; 12(4):502-7. doi:10.1128/CDLI.12.4.502-507.2005 PMID: 15817757; PubMed Central PMCID: PMCPMC1074380.
11. World Health Organization tPR. Leishmaniasis. In: Organization WH, editor. Tropcial Disease Research 20 Years of Progress Geneva: World Health Organization; 1995. p. 135-46.
12. Redmond HP, Leon P, Lieberman MD, Hofmann K, Shou J, Reynolds JV, et al. Impaired macrophage function in severe protein-energy malnutrition. Arch Surg. 1991; 126(2):192-6. PMID: 1847038.
13. de la Fuente M, Munoz ML. Impairment of phagocytic process in macrophages from young and old mice by protein malnutrition. Ann Nutr Metab. 1992; 36(1):41-7. PMID: 1590671.
14. Schaffer MR, Tantry U, Ahrendt GM, Wasserkrug HL, Barbul A. Acute protein-calorie malnutrition impairs wound healing: A possible role of decreased wound nitric oxide synthesis. J Am Coll Surg. 1997; 184(1):37-43. PMID: 8989298.
15. Fock RA, Rogero MM, Vinolo MA, Curi R, Borges MC, Borelli P. Effects of protein-energy malnutrition on NF-kappaB signalling in murine peritoneal macrophages. Inflammation. 2010; 33(2):101-9. doi:10.1007/s10753-009-9163-x PMID: 19876726.
16. Qadri F, Bhuiyan TR, Sack DA, Svennerholm AM. Immune responses and protection in children in developing countries induced by oral vaccines. Vaccine. 2013; 31(3):452-60. doi:10.1016/j.vaccine.2012.11.012 PMID: 23153448.
17. Tomkins AM, Dunn DT, Hayes RJ. Nutritional status and risk of morbidity among young Gambian children allowing for social and environmental factors. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1989; 83(2):282-7. PMID: 2609387.
18. Chandra RK. Nutrition and immunology: from the clinic to cellular biology and back again. Proc Nutr Soc. 1999; 58(3):681-3. PMID: 10604203.
19. Muller O, Krawinkel M. Malnutrition and health in developing countries. CMAJ. 2005; 173(3):279-86. doi:10.1503/cmaj.050342 PMID: 16076825; PubMed Central PMCID: PMCPMC1180662.
20. Marcos A, Nova E, Montero A. Changes in the immune system are conditioned by nutrition. Eur J Clin Nutr. 2003; 57 Suppl 1:S66-9. doi: 10.1038/sj.ejcn.1601819 PMID: 12947457.
21. Malnutrition in the community and hospital setting 2011. Available: http://www.patients-association.com/Portals/0/Public/Files/AdvicePublications/Malnutritioninthecommunityandhosptialsettting.pdf.
22. Takele Y, Abebe T, Weldegebreal T, Hailu A, Hailu W, Hurissa Z, et al. Arginase activity in the blood of patients with visceral leishmaniasis and HIV infection. PLOS Negl Trop Dis. 2013; 7(1):e1977. doi:10.1371/journal.pntd.0001977 PMID: 23349999; PubMed Central PMCID: PMC3547864.
23. Abebe T, Takele T, Weldegebreal T, Cloke T, Closs E, Corset C, et al. Arginase: A marker of disease status in patients with visceral leishmaniasis. Plos Ntd. 2013; 7(3):e2134.
24. Nylen S, Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol. 2007; 28(9):378-84. PMID: 17689290.
25. Goto H, Prianti MG. Immunoactivation and immunopathogeny during active visceral leishmaniasis. Rev Inst Med Trop Sao Paulo. 2009; 51(5):241-6. Epub 2009/11/07. S0036-46652009000500002 [pii]. PMID: 19893975.
26. Branca F, Pastore G, Demissie T, Ferro-Luzzi A. The nutritional impact of seasonality in children and adults of rural Ethiopia. Eur J Clin Nutr. 1993; 47(12):840-50. PMID: 8156981.
27. Kropf P, Baud D, Marshall SE, Munder M, Mosley A, Fuentes JM, et al. Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur J Immunol. 2007; 37(4):935-45. Epub 2007/03/03. doi:10.1002/eji.200636542 PMID: 17330821; PubMed Central PMCID: PMC2699382.
28. Dubois B, Vanbervliet B, Fayette J, Massacrier C, van Kooten C, Briere F, et al. Dendritic cells enhance growth and differentiation of CD40-activated B lymphocytes.!!! BADKEY-Journal Name Lost. 1997; 25934:26988-11635.
29. Wasunna KM, Raynes JG, Were JB, Muigai R, Sherwood J, Gachihi G, et al. Acute phase protein concentrations predict parasite clearance rate during therapy for visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1995; 89(6):678-81. PMID: 8594695.
30. Kropf P, Fuentes JM, Fahnrich E, Arpa L, Herath S, Weber V, et al. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. Faseb J. 2005; 19:1000-2. PMID: 15811879.
31. Marcos A, Varela P, Santacruz I, Munoz-Velez A, Morande G. Nutritional status and immunocompetence in eating disorders. A comparative study. Eur J Clin Nutr. 1993; 47(11):787-93. PMID: 8287848.
32. Chandra RK. Nutrition and the immune system from birth to old age. Eur J Clin Nutr. 2002; 56 Suppl 3: S73-6. doi: 10.1038/sj.ejcn.1601492 PMID: 12142969.
33. Munder M. Arginase: An emerging key player in the mammalian immune system. Br J Pharmacol. 2009; 158(3):638-51. Epub 2009/09/22. BPH291 [pii] doi:10.1111/j.1476-5381.2009.00291.x PMID: 19764983; PubMed Central PMCID: PMC2765586.
34. Cloke T, Garvery L, Choi BS, Abebe T, Hailu A, Hancock M, et al. Increased arginase activity correlates with disease severity in HIV seropositive patients. Journal of Infectious Diseases. 2010; 202:374-85. doi:10.1086/653736 PMID: 20575659.
35. Corware K, Yardley V, Mack C, Schuster S, Al-Hassi H, Herath S, et al. Protein energy malnutrition increases arginase activity in monocytes and macrophages. Nutr Metab (Lond). 2014; 11(1):51. doi:10.1186/1743-7075-11-51 PMID: 25392710; PubMed Central PMCID: PMCPMC4228191.
36. Kuijpers TW, Tool AT, van der Schoot CE, Ginsel LA, Onderwater JJ, Roos D, et al. Membrane surface antigen expression on neutrophils: A reappraisal of the use of surface markers for neutrophil activation. Blood. 1991; 78(4):1105-11. Epub 1991/08/15. PMID: 1907873.
37. Thakur N, Chandra J, Pemde H, Singh V. Anemia in severe acute malnutrition. Nutrition. 2014; 30 (4):440-2. doi:10.1016/j.nut.2013.09.011 PMID: 24332525.
38. Adams EB. Anemia associated with kwashiorkor. Am J Clin Nutr. 1969; 22(12):1634-8. PMID: 5395474.
39. Hutter G, Ganepola S, Hofmann WK. The hematology of anorexia nervosa. Int J Eat Disord. 2009; 42 (4):293-300. doi:10.1002/eat.20610 PMID: 19040272.
40. http://www.who.int/mediacentre/factsheets/fs375/fr/Leishmaniose 2014.
41. White JV, Guenter P, Jensen G, Malone A, Schofield M, Academy Malnutrition Work G, et al. Consensus statement: Academy of Nutrition and Dietetics and American Society for Parenteral and Enteral Nutrition: characteristics recommended for the identification and documentation of adult malnutrition (undernutrition). JPEN J Parenter Enteral Nutr. 2012; 36(3):275-83. doi:10.1177/0148607112440285 PMID: 22535923.
42. Solmi M, Veronese N, Favaro A, Santonastaso P, Manzato E, Sergi G, et al. Inflammatory cytokines and anorexia nervosa: A meta-analysis of cross-sectional and longitudinal studies. Psychoneuroendocrinology. 2015; 51:237-52. doi:10.1016/j.psyneuen.2014.09.031 PMID: 25462897.
43. Molofsky AB, Savage AK, Locksley RM. Interleukin-33 in Tissue Homeostasis, Injury, and Inflammation. Immunity. 2015; 42(6):1005-19. doi:10.1016/j.immuni.2015.06.006 PMID: 26084021; PubMed Central PMCID: PMCPMC4471869.
44. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ. 2005; 12 Suppl 2:1542-52. doi: 10.1038/sj.cdd.4401765 PMID: 16247502; PubMed Central PMCID: PMCPMC1828868.
45. Altman BJ, Rathmell JC. Metabolic stress in autophagy and cell death pathways. Cold Spring Harb Perspect Biol. 2012; 4(9):a008763. doi:10.1101/cshperspect.a008763 PMID: 22952396; PubMed Central PMCID: PMCPMC3428762.
46. Kheloufi M, Boulanger CM, Durand F, Rautou PE. Liver autophagy in anorexia nervosa and acute liver injury. Biomed Res Int. 2014; 2014:701064. doi:10.1155/2014/701064 PMID: 25250330; PubMed Central PMCID: PMCPMC4163421.
47. Ma Y, Galluzzi L, Zitvogel L, Kroemer G. Autophagy and cellular immune responses. Immunity. 2013; 39(2):211-27. doi:10.1016/j.immuni.2013.07.017 PMID: 23973220.
48. Perez-Mazliah D, Langhorne J. CD4 T-cell subsets in malaria: TH1/TH2 revisited. Front Immunol. 2014; 5:671. doi:10.3389/fimmu.2014.00671 PMID: 25628621; PubMed Central PMCID: PMCPMC4290673.
49. Muller I, Munder M, Kropf P, Hansch GM. Polymorphonuclear neutrophils and T lymphocytes: strange bedfellows or brothers in arms? Trends Immunol. 2009; 30(11):522-30. Epub 2009/09/25. S1471-4906 (09)00139-2 [pii] doi:10.1016/j.it.2009.07.007 PMID: 19775938.
50. Bowers NL, Helton ES, Huijbregts RP, Goepfert PA, Heath SL, Hel Z. Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. Plos Pathog. 2014; 10(3):e1003993. doi:10.1371/journal.ppat.1003993 PMID: 24626392; PubMed Central PMCID: PMCPMC3953441.