×

zbMATH — the first resource for mathematics

A mathematical model for the macrophage response to respiratory viral infection in normal and asthmatic conditions. (English) Zbl 1372.92058
Summary: Respiratory viral infections are common in the general population and one of the most important causes of asthma aggravation and exacerbation. Despite many studies, it is not well understood how viral infections cause more severe symptoms and exacerbations in asthmatics. We develop a mathematical model of two types of macrophages that play complementary roles in fighting viral infection: classically (CA-\(\mathrm M\Phi\)) and alternatively activated macrophages (AA-\(\mathrm M\Phi\)). (CA-\(\mathrm M\Phi\)) destroy infected cells and tissues to remove viruses, while (AA-\(\mathrm M\Phi\)) repair damaged tissues. We show that a higher viral load or longer duration of infection provokes a stronger immune response from the macrophage system. By adjusting the parameters, we model the differences in response to respiratory viral infection in normal and asthmatic subjects and show how this skews the system toward a response that generates more severe symptoms in asthmatic patients.
MSC:
92C60 Medical epidemiology
92C50 Medical applications (general)
Software:
deSolve; diffEq; R
PDF BibTeX XML Cite
Full Text: DOI
References:
[1] Akaike, T; Fujii, S; Kato, A; etal., Viral mutation accelerated by nitric oxide production during infection in vivo, Faseb J, 14, 1447-1454, (2000)
[2] Boukhvalova, MS; Prince, GA; Soroush, L; Harrigan, DC; Vogel, SN; Blanco, JC, The TLR4 agonist, monophosphoryl lipid A, attenuates the cytokine storm associated with respiratory syncytial virus vaccine-enhanced disease, Vaccine, 24, 5027-5035, (2006)
[3] Broide, DH; Lotz, M; Cuomo, AJ; Coburn, DA; Federman, EC; Wasserman, SI, Cytokines in symptomatic asthma airways, J Allergy Clin Immunol, 89, 958-967, (1992)
[4] Busse, WW; Lemanske, RF; Gern, JE, Role of viral respiratory infections in asthma and asthma exacerbations, Lancet, 376, 826-834, (2010)
[5] Chernyavsky, IL; Croisier, H; Chapman, LA; etal., The role of inflammation resolution speed in airway smooth muscle mass accumulation in asthma: insight from a theoretical model, PLoS One, 9, e90162, (2014)
[6] Childs, LM; Paskow, M; Morris, SM; Hesse, M; Strogatz, S, From inflammation to wound healing: using a simple model to understand the functional versatility of murine macrophages, Bull Math Biol, 73, 2575-2604, (2011) · Zbl 1334.92193
[7] Contoli, M; Message, SD; Laza-Stanca, V; etal., Role of deficient type III interferon-lambda production in asthma exacerbations, Nat Med, 12, 1023-1026, (2006)
[8] Corne, JM; Marshall, C; Smith, S; etal., Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study, Lancet, 359, 831-834, (2002)
[9] Curran, JN; Winter, DC; Bouchier-Hayes, D, Biological fate and clinical implications of arginine metabolism in tissue healing, Wound Repair Regen, 14, 376-386, (2006)
[10] Development Core Team R (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
[11] DeVincenzo, JP; Wilkinson, T; Vaishnaw, A; etal., Viral load drives disease in humans experimentally infected with respiratory syncytial virus, Am J Respir Crit Care Med, 182, 1305-1314, (2010)
[12] Dolin, R; Kasper, DL (ed.); etal., Common viral respiratory infections, 1205-1209, (2015), New York
[13] Dougherty, RH; Fahy, JV, Acute exacerbations of asthma: epidemiology, biology and the exacerbation-prone phenotype, Clin Exp Allergy, 39, 193-202, (2009)
[14] Dweik, RA; Boggs, PB; Erzurum, SC; etal., An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications, Am J Respir Crit Care Med, 184, 602-615, (2011)
[15] Saleeby, CM; Bush, AJ; Harrison, LM; Aitken, JA; Devincenzo, JP, Respiratory syncytial virus load, viral dynamics, and disease severity in previously healthy naturally infected children, J Infect Dis, 204, 996-1002, (2011)
[16] Erdman, DD; Weinberg, GA; Edwards, KM; etal., Genescan reverse transcription-PCR assay for detection of six common respiratory viruses in Young children hospitalized with acute respiratory illness, J Clin Microbiol, 41, 4298-4303, (2003)
[17] Folcik, VA; An, GC; Orosz, CG, The basic immune simulator: an agent-based model to study the interactions between innate and adaptive immunity, Theor Biol Med Model, 4, 39, (2007)
[18] Gehlhar, K; Bilitewski, C; Reinitz-Rademacher, K; Rohde, G; Bufe, A, Impaired virus-induced interferon-alpha2 release in adult asthmatic patients, Clin Exp Allergy, 36, 331-337, (2006)
[19] GINA (2014) Global strategy for asthma management and prevention, global initiative for asthma (GINA) 2014. Available from: http://www.ginasthma.org/. Date last updated. 2014
[20] Haldar, P; Pavord, ID; Shaw, DE; etal., Cluster analysis and clinical asthma phenotypes, Am J Respir Crit Care Med, 178, 218-224, (2008)
[21] Holt, PG; Rowe, J; Kusel, M; etal., Toward improved prediction of risk for atopy and asthma among preschoolers: a prospective cohort study, J Allergy Clin Immunol, 125, 653-659, (2010)
[22] Hussell, T; Bell, TJ, Alveolar macrophages: plasticity in a tissue-specific context, Nat Rev Immunol, 14, 81-93, (2014)
[23] Hussell, T; Spender, LC; Georgiou, A; O’Garra, A; Openshaw, PJ, Th1 and th2 cytokine induction in pulmonary T cells during infection with respiratory syncytial virus, J Gen Virol, 77, 2447-2455, (1996)
[24] Iikura, K; Katsunuma, T; Saika, S; etal., Peripheral blood mononuclear cells from patients with bronchial asthma show impaired innate immune responses to rhinovirus in vitro, Int Arch Allergy Immunol, 155, 27-33, (2011)
[25] Jackson, DJ; Gangnon, RE; Evans, MD; etal., Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children, Am J Respir Crit Care Med, 178, 667-672, (2008)
[26] Jackson, DJ; Johnston, SL, The role of viruses in acute exacerbations of asthma, J Allergy Clin Immunol, 125, 1178-1187, (2010)
[27] Jacoby, DB, Virus-induced asthma attacks, J Aerosol Med, 17, 169-173, (2004)
[28] Jiang, H; Harris, MB; Rothman, P, IL-4/IL-13 signaling beyond JAK/STAT, J Allergy Clin Immunol, 105, 1063-1070, (2000)
[29] Karupiah, G; Chen, JH; Mahalingam, S; Nathan, CF; MacMicking, JD, Rapid interferon gamma-dependent clearance of influenza A virus and protection from consolidating pneumonitis in nitric oxide synthase 2-deficient mice, J Exp Med, 188, 1541-1546, (1998)
[30] Khaitov, MR; Laza-Stanca, V; Edwards, MR; etal., Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells, Allergy, 64, 375-386, (2009)
[31] Khallou-Laschet, J; Varthaman, A; Fornasa, G; etal., Macrophage plasticity in experimental atherosclerosis, PLoS One, 5, e8852, (2010)
[32] Kharitonov, SA; Yates, D; Barnes, PJ, Increased nitric oxide in exhaled air of normal human subjects with upper respiratory tract infections, Eur Respir J, 8, 295-297, (1995)
[33] Kim, CK; Kim, SW; Park, CS; Kim, BI; Kang, H; Koh, YY, Bronchoalveolar lavage cytokine profiles in acute asthma and acute bronchiolitis, J Allergy Clin Immunol, 112, 64-71, (2003)
[34] Kim, Y; Lee, S; Kim, YS; etal., Regulation of th1/th2 cells in asthma development: a mathematical model, Math Biosci Eng, 10, 1095-1133, (2013) · Zbl 1273.92024
[35] Kleiner, G; Marcuzzi, A; Zanin, V; Monasta, L; Zauli, G, Cytokine levels in the serum of healthy subjects, Mediat Inflamm, 2013, 434010, (2013)
[36] Kolodziejski, PJ; Koo, JS; Eissa, NT, Regulation of inducible nitric oxide synthase by rapid cellular turnover and cotranslational down-regulation by dimerization inhibitors, Proc Natl Acad Sci USA, 101, 18141-18146, (2004)
[37] Kusel, MM; Klerk, NH; Kebadze, T; etal., Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma, J Allergy Clin Immunol, 119, 1105-1110, (2007)
[38] McKenna, SD; Vergilis, K; Arulanandam, AR; Weiser, WY; Nabioullin, R; Tepper, MA, Formation of human IFN-beta complex with the soluble type I interferon receptor IFNAR-2 leads to enhanced IFN stability, pharmacokinetics, and antitumor activity in xenografted SCID mice, J Interferon Cytokine Res, 24, 119-129, (2004)
[39] Modolell, M; Corraliza, IM; Link, F; Soler, G; Eichmann, K, Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines, Eur J Immunol, 25, 1101-1104, (1995)
[40] Moore, WC; Meyers, DA; Wenzel, SE; etal., Identification of asthma phenotypes using cluster analysis in the severe asthma research program, Am J Respir Crit Care Med, 181, 315-323, (2009)
[41] Murphy, J; Summer, R; Wilson, AA; Kotton, DN; Fine, A, The prolonged life-span of alveolar macrophages, Am J Respir Cell Mol Biol, 38, 380-385, (2008)
[42] Proud, D; Chow, CW, Role of viral infections in asthma and chronic obstructive pulmonary disease, Am J Respir Cell Mol Biol, 35, 513-518, (2006)
[43] Rath, M; Muller, I; Kropf, P; Closs, EI; Munder, M, Metabolism via arginase or nitric oxide synthase: two competing arginine pathways in macrophages, Front Immunol, 5, 532, (2014)
[44] Richardson, JY; Ottolini, MG; Pletneva, L; etal., Respiratory syncytial virus (RSV) infection induces cyclooxygenase 2: a potential target for RSV therapy, J Immunol, 174, 4356-4364, (2005)
[45] Shaykhiev, R; Krause, A; Salit, J; etal., Smoking-dependent reprogramming of alveolar macrophage polarization: implication for pathogenesis of chronic obstructive pulmonary disease, J Immunol, 183, 2867-2883, (2009)
[46] Shirey, KA; Pletneva, LM; Puche, AC; etal., Control of RSV-induced lung injury by alternatively activated macrophages is IL-4R alpha-, TLR4-, and IFN-beta-dependent, Mucosal Immunol, 3, 291-300, (2010)
[47] Smith, AM; Adler, FR; Perelson, AS, An accurate two-phase approximate solution to an acute viral infection model, J Math Biol, 60, 711-726, (2010) · Zbl 1198.92029
[48] Soetaert, K; Petzoldt, T; Setzer, RW, Solving differential equations in R: package desolve, J Stat Softw, 33, 1-25, (2010)
[49] Song, L; Guo, Y; Deng, Q; Li, J, TH17 functional study in severe asthma using agent based model, J Theor Biol, 309, 29-33, (2012) · Zbl 1411.92067
[50] Sturzebecher, S; Maibauer, R; Heuner, A; Beckmann, K; Aufdembrinke, B, Pharmacodynamic comparison of single doses of IFN-beta1a and IFN-beta1b in healthy volunteers, J Interferon Cytokine Res, 19, 1257-1264, (1999)
[51] Sumi, Y; Hamid, Q, Airway remodeling in asthma, Allergol Int, 56, 341-348, (2007)
[52] Syrmis, MW; Whiley, DM; Thomas, M; etal., A sensitive, specific, and cost-effective multiplex reverse transcriptase-PCR assay for the detection of seven common respiratory viruses in respiratory samples, J Mol Diagn, 6, 125-131, (2004)
[53] Takaoka, A; Hayakawa, S; Yanai, H; etal., Integration of interferon-alpha/beta signalling to p53 responses in tumour suppression and antiviral defence, Nature, 424, 516-523, (2003)
[54] Tsutsumi, H; Takeuchi, R; Ohsaki, M; Seki, K; Chiba, S, Respiratory syncytial virus infection of human respiratory epithelial cells enhances inducible nitric oxide synthase gene expression, J Leukoc Biol, 66, 99-104, (1999)
[55] oud Alblas, AB; Furth, R, Origin, kinetics, and characteristics of pulmonary macrophages in the normal steady state, J Exp Med, 149, 1504-1518, (1979)
[56] Virchow, JC; Walker, C; Hafner, D; etal., T cells and cytokines in bronchoalveolar lavage fluid after segmental allergen provocation in atopic asthma, Am J Respir Crit Care Med, 151, 960-968, (1995)
[57] Wark, PA; Grissell, T; Davies, B; See, H; Gibson, PG, Diversity in the bronchial epithelial cell response to infection with different rhinovirus strains, Respirology, 14, 180-186, (2009)
[58] Wark, PA; Johnston, SL; Bucchieri, F; etal., Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus, J Exp Med, 201, 937-947, (2005)
[59] Weigl, JA; Puppe, W; Grondahl, B; Schmitt, HJ, Epidemiological investigation of nine respiratory pathogens in hospitalized children in Germany using multiplex reverse-transcriptase polymerase chain reaction, Eur J Clin Microbiol Infect Dis, 19, 336-343, (2000)
[60] Wink, DA; Hines, HB; Cheng, RY; etal., Nitric oxide and redox mechanisms in the immune response, J Leukoc Biol, 89, 873-891, (2011)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. It attempts to reflect the references listed in the original paper as accurately as possible without claiming the completeness or perfect precision of the matching.