Cryptococcus gattii Infection as the Major Clinical Manifestation in Patients with Autoantibodies Against Granulocyte-Macrophage Colony-Stimulating Factor.


Journal

Journal of clinical immunology
ISSN: 1573-2592
Titre abrégé: J Clin Immunol
Pays: Netherlands
ID NLM: 8102137

Informations de publication

Date de publication:
11 2022
Historique:
received: 23 02 2022
accepted: 20 07 2022
pubmed: 11 8 2022
medline: 30 11 2022
entrez: 10 8 2022
Statut: ppublish

Résumé

Anti-granulocyte-macrophage colony-stimulating factor autoantibodies (anti-GM-CSF Abs) are a predisposing factor for pulmonary alveolar proteinosis (PAP) and Cryptococcus gattii cryptococcosis. This study aimed to investigate clinical manifestations in anti-GM-CSF Ab-positive patients with C. gattii cryptococcosis and analyze the properties of anti-GM-CSF Abs derived from these patients and patients with PAP. Thirty-nine patients diagnosed with cryptococcosis (caused by C. neoformans or C. gattii) and 6 with PAP were enrolled in the present study. Clinical information was obtained from medical records. Blood samples were collected for analysis of autoantibody properties. We also explored the National Health Insurance Research Database (NHIRD) of Taiwan to investigate the epidemiology of cryptococcosis and PAP. High titers of neutralizing anti-GM-CSF Abs were identified in 15 patients with cryptococcosis (15/39, 38.5%). Most anti-GM-CSF Ab-positive cryptococcosis cases had central nervous system (CNS) involvement (14/15, 93.3%). Eleven out of 14 (78.6%) anti-GM-CSF Ab-positive CNS cryptococcosis patients were confirmed to be infected with C. gattii, and PAP did not occur synchronously or metachronously in a single patient from our cohort. Exploration of an association between HLA and anti-GM-CSF Ab positivity or differential properties of autoantibodies from cryptococcosis patients and PAP yielded no significant results. Anti-GM-CSF Abs can cause two diseases, C. gattii cryptococcosis and PAP, which seldom occur in the same subject. Current biological evidence regarding the properties of anti-GM-CSF Abs cannot provide clues regarding decisive mechanisms. Further analysis, including more extensive cohort studies and investigations into detailed properties, is mandatory to better understand the pathogenesis of anti-GM-CSF Abs.

Identifiants

pubmed: 35947322
doi: 10.1007/s10875-022-01341-2
pii: 10.1007/s10875-022-01341-2
doi:

Substances chimiques

Autoantibodies 0
Granulocyte-Macrophage Colony-Stimulating Factor 83869-56-1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1730-1741

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Browne SK. Anticytokine autoantibody-associated immunodeficiency. Annu Rev Immunol. 2014;1(32):635–57.
doi: 10.1146/annurev-immunol-032713-120222
Ku CL, Chi CY, von Bernuth H, Doffinger R. Autoantibodies against cytokines: phenocopies of primary immunodeficiencies? Hum Genet. 2020;139(6–7):783–94.
pubmed: 32419033 pmcid: 7272486 doi: 10.1007/s00439-020-02180-0
Vincent T, Plawecki MM, Goulabchand R, Guilpain P, Eliaou JFF. Emerging clinical phenotypes associated with anti-cytokine autoantibodies. Autoimmun Rev. 2015;14(6):528–35.
pubmed: 25633324 doi: 10.1016/j.autrev.2015.01.015
Shih HP, Ding JY, Yeh CF, Chi CY, Ku CL. Anti-interferon-γ autoantibody-associated immunodeficiency. Curr Opin Immunol. 2021;72:206–14.
pubmed: 34175547 doi: 10.1016/j.coi.2021.05.007
Ben-Dov I, Segel MJ. Autoimmune pulmonary alveolar proteinosis: clinical course and diagnostic criteria. Autoimmun Rev. 2014;13(4–5):513–7.
pubmed: 24424195 doi: 10.1016/j.autrev.2014.01.046
Kitamura T, Tanaka N, Watanabe J, Uchida K, Kanegasaki S, Yamada Y, et al. Idiopathic pulmonary alveolar proteinosis as an autoimmune disease with neutralizing antibody against granulocyte/macrophage colony-stimulating factor. J Exp Med. 1999;190(6):875–80.
pubmed: 10499925 pmcid: 2195627 doi: 10.1084/jem.190.6.875
Hildebrandt J, Yalcin E, Bresser H-G, Cinel G, Gappa M, Haghighi A, et al. Characterization of CSF2RA mutation related juvenile pulmonary alveolar proteinosis. Orphanet J Rare Dis. 2014;9:171.
pubmed: 25425184 pmcid: 4254258 doi: 10.1186/s13023-014-0171-z
Suzuki T, Maranda B, Sakagami T, Catellier P, Couture C-Y, Carey BC, et al. Hereditary pulmonary alveolar proteinosis caused by recessive CSF2RB mutations. Vol. 37, The European respiratory journal. England; 2011. p. 201–4.
Uchida K, Nakata K, Trapnell BC, Terakawa T, Hamano E, Mikami A, et al. High-affinity autoantibodies specifically eliminate granulocyte-macrophage colony-stimulating factor activity in the lungs of patients with idiopathic pulmonary alveolar proteinosis. Blood. 2004;103(3):1089–98.
pubmed: 14512323 doi: 10.1182/blood-2003-05-1565
Morales-López SE, Garcia-Effron G. Infections due to rare Cryptococcus species. A literature review J Fungi. 2021;7(4):1–20.
Tseng HK, Liu CP, Ho MW, Lu PL, Lo HJ, Lin YH, et al. Microbiological, epidemiological, and clinical characteristics and outcomes of patients with cryptococcosis in Taiwan, 1997–2010. PLoS One. 2013;8(4).
Rosen LB, Freeman AF, Yang LM, Jutivorakool K, Olivier KN, Angkasekwinai N, et al. Anti–GM-CSF autoantibodies in patients with cryptococcal Meningitis. J Immunol. 2013;190(8):3959–66.
pubmed: 23509356 doi: 10.4049/jimmunol.1202526
Saijo T, Chen J, Chen SC-ACA, Rosen LB, Yi J, Sorrell TC, et al. Anti-granulocyte-macrophage colony-stimulating factor autoantibodies are a risk factor for central nervous system infection by Cryptococcus gattii in otherwise immunocompetent patients. MBio. 2014;5(2):e00912-14.
pubmed: 24643864 pmcid: 3967522 doi: 10.1128/mBio.00912-14
Kuo C-YC-Y, Wang S-YS-Y, Shih H-PH-PH-P, Tu K-HK-H, Huang W-CW-CW-C, Ding J-YJ-Y, et al. Disseminated cryptococcosis due to anti-granulocyte-macrophage colony-stimulating factor autoantibodies in the absence of pulmonary alveolar proteinosis. J Clin Immunol. 2017;37(2):143–52.
pubmed: 28013480 doi: 10.1007/s10875-016-0364-4
Crum-Cianflone NF, Lam PV, Ross-Walker S, Rosen LB, Holland SM. Autoantibodies to granulocyte-macrophage colony-stimulating factor associated with severe and unusual manifestations of Cryptococcus gattii infections. Open Forum Infect Dis. 2017;4(4):1–6.
doi: 10.1093/ofid/ofx211
Applen Clancey S, Ciccone EJ, Coelho MA, Davis J, Ding L, Betancourt R, et al. Cryptococcus deuterogattii vgiia infection associated with travel to the pacific northwest outbreak region in an anti- granulocyte-macrophage colony-stimulating factor autoantibody-positive patient in the united states. MBio. 2019;10(1):e02733-e2818.
pubmed: 30755511 pmcid: 6372798 doi: 10.1128/mBio.02733-18
Kuo PH, Wu UI, Pan YH, Wang JT, Wang YC, Sun HY, et al. Neutralizing anti-GM-CSF autoantibodies in patients with CNS and localized cryptococcosis: a longitudinal follow-up and literature review. Clin Infect Dis. 2021; ciab920.
Yang DH, England MR, Salvator H, Anjum S, Park YD, Marr KA, et al. Cryptococcus gattii species complex as an opportunistic pathogen: underlying medical conditions associated with the infection. MBio. 2021;12(5):e0270821.
pubmed: 34700378 doi: 10.1128/mBio.02708-21
Rosen LB, Rocha Pereira N, Figueiredo C, Fiske LC, Ressner RA, Hong JC, et al. Nocardia-induced granulocyte macrophage colony-stimulating factor is neutralized by autoantibodies in disseminated/extrapulmonary nocardiosis. Clin Infect Dis. 2015;60(7):1017–25.
pubmed: 25472947 doi: 10.1093/cid/ciu968
Carey B, Trapnell BC. The molecular basis of pulmonary alveolar proteinosis. Clin Immunol. 2010;135(2):223–35.
pubmed: 20338813 pmcid: 2866141 doi: 10.1016/j.clim.2010.02.017
Lim WT, Mudalige S, Nilushi T, Shanka J, Parakrama K. Crazy-paving pattern: a rare case of autoimmune pulmonary alveolar proteinosis (PAP) with positive anti-GM-CSF antibody following cryptococcal infection in an otherwise healthy individual and review of literature. Eur J Respir Med. 2021;3(2):200–5.
Peter Donnelly J, Chen SC, Kauffman CA, Steinbach WJ, Baddley JW, Verweij PE, et al. Revision and update of the consensus definitions of invasive fungal disease from the European organization for research and treatment of cancer and the mycoses study group education and research consortium. Clin Infect Dis. 2020;71(6):1367–76.
pubmed: 31802125 doi: 10.1093/cid/ciz1008
Maziarz EK, Perfect JR. Cryptococcosis. Infect Dis Clin North Am. 2016;30(1):179–206.
pubmed: 26897067 pmcid: 5808417 doi: 10.1016/j.idc.2015.10.006
Quelle FW, Sato N, Witthuhn BA, Inhorn RC, Eder M, Miyajima A, et al. JAK2 associates with the beta c chain of the receptor for granulocyte-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol Cell Biol. 1994;14(7):4335–41.
pubmed: 8007942 pmcid: 358804
Mui AL, Wakao H, O’Farrell AM, Harada N, Miyajima A. Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two STAT5 homologs. EMBO J. 1995;14(6):1166–75.
pubmed: 7720707 pmcid: 398194 doi: 10.1002/j.1460-2075.1995.tb07100.x
Kitamura T, Tange T, Terasawa T, Chiba S, Kuwaki T, Miyagawa K, et al. Establishment and characterization of a unique human cell line that proliferates dependently on GM-CSF, IL-3, or erythropoietin. J Cell Physiol. 1989;140(2):323–34.
pubmed: 2663885 doi: 10.1002/jcp.1041400219
Lin KH, Chen CM, Chen TL, Kuo SC, Kao CC, Jeng YC, et al. Diabetes mellitus is associated with acquisition and increased mortality in HIV-uninfected patients with cryptococcosis: a population-based study. J Infect. 2016;72(5):608–14.
pubmed: 26920792 doi: 10.1016/j.jinf.2016.01.016
Ku CL, Lin CH, Chang SW, Chu CC, Chan JFW, Kong XF, et al. Anti–IFN-γ autoantibodies are strongly associated with HLA-DR*15:02/16:02 and HLA-DQ*05:01/05:02 across Southeast Asia. J Allergy Clin Immunol. 2016;137(3):945-948.e8.
pubmed: 26522403 doi: 10.1016/j.jaci.2015.09.018
Chen PL, Fann CSJ, Chu CC, Chang CC, Chang SW, Hsieh HY, et al. Comprehensive genotyping in two homogeneous Graves’ disease samples reveals major and novel HLA association alleles. PLoS One. 2011;6(1):10–4.
pmcid: 3228704 doi: 10.1371/journal.pone.0016635
Chi CY, Chu CC, Liu JP, Lin CH, Ho MW, Lo WJ, et al. Anti-IFN-gamma autoantibodies in adults with disseminated nontuberculous mycobacterial infections are associated with HLA-DRB1*16:02 and HLA-DQB1*05:02 and the reactivation of latent varicella-zoster virus infection. Blood. 2013;121(8):1357–66.
pubmed: 23243276 doi: 10.1182/blood-2012-08-452482
Sakaue S, Yamaguchi E, Inoue Y, Takahashi M, Hirata J, Suzuki K, et al. Genetic determinants of risk in autoimmune pulmonary alveolar proteinosis. Nat Commun. 2021;12(1):1032.
pubmed: 33589587 pmcid: 7884840 doi: 10.1038/s41467-021-21011-y
Piccoli L, Campo I, Fregni CS, Rodriguez BMF, Minola A, Sallusto F, et al. Neutralization and clearance of GM-CSF by autoantibodies in pulmonary alveolar proteinosis. Nat Commun. 2015;6:7375.
pubmed: 26077231 doi: 10.1038/ncomms8375
Wormley FL, Perfect JR, Steele C, Cox GM. Protection against cryptococcosis by using a murine gamma interferon-producing Cryptococcus neoformans strain. Infect Immun. 2007;75(3):1453–62.
pubmed: 17210668 pmcid: 1828544 doi: 10.1128/IAI.00274-06
Chen GH, McDonald RA, Wells JC, Huffnagle GB, Lukacs NW, Toews GB. The gamma interferon receptor is required for the protective pulmonary inflammatory response to Cryptococcus neoformans. Infect Immun. 2005;73(3):1788–96.
pubmed: 15731080 pmcid: 1064966 doi: 10.1128/IAI.73.3.1788-1796.2005
Chetchotisakd P, Anunnatsiri S, Nithichanon A, Lertmemongkolchai G. Cryptococcosis in anti-interferon-gamma autoantibody-positive patients: a different clinical manifestation from HIV-infected patients. Jpn J Infect Dis. 2017;70(1):69–74.
pubmed: 27169938 doi: 10.7883/yoken.JJID.2015.340
Chi CY, Lin CH, Ho MW, Ding JY, Huang WC, Shih HP, et al. Clinical manifestations, course, and outcome of patients with neutralizing anti-interferon-γ autoantibodies and disseminated nontuberculous mycobacterial infections. Medicine (Baltimore). 2016;95(25):e3927.
pubmed: 27336882 doi: 10.1097/MD.0000000000003927
de Souza TL, de SC Fernandes RC, da Silva JA, Alves VG, Coelho AG, Faria ACS, et al. Microbial disease spectrum linked to a novel IL-12Rβ1 N-terminal signal peptide stop-gain homozygous mutation with paradoxical receptor cell-surface expression. Front Microbiol. 2017;8:1–10.
Wipasa J, Chaiwarith R, Chawansuntati K, Praparattanapan J, Rattanathammethee K, Supparatpinyo K. Characterization of anti-interferon-γ antibodies in HIV-negative immunodeficient patients infected with unusual intracellular microorganisms. Exp Biol Med. 2018;243(7):621–6.
doi: 10.1177/1535370218764086
Decken K, Köhler G, Palmer-Lehmann K, Wunderlin A, Mattner F, Magram J, et al. Interleukin-12 is essential for a protective Th1 response in mice infected with Cryptococcus neoformans. Infect Immun. 1998;66(10):4994–5000.
pubmed: 9746609 pmcid: 108620 doi: 10.1128/IAI.66.10.4994-5000.1998
Jirapongsananuruk O, Luangwedchakarn V, Niemela JE, Pacharn P, Visitsunthorn N, Thepthai C, et al. Cryptococcal osteomyelitis in a child with a novel compound mutation of the IL12RB1 gene. Asian Pacific J allergy Immunol. 2012;30(1):79–82.
Rezai MS, Khotael G, Kheirkhah M, Hedayat T, Geramishoar M, Mahjoub F. Cryptococcosis and deficiency of interleukin12r. Vol. 27, The Pediatric infectious disease journal. United States; 2008. p. 673.
Amorim A, De Feo D, Friebel E, Ingelfinger F, Anderfuhren CD, Krishnarajah S, et al. IFNγ and GM-CSF control complementary differentiation programs in the monocyte-to-phagocyte transition during neuroinflammation. Nat Immunol. 2022;23(2):217–28.
pubmed: 35102344 doi: 10.1038/s41590-021-01117-7
Chitu V, Biundo F, Stanley ER. Colony stimulating factors in the nervous system. Semin Immunol. 2021;54:101511.
pubmed: 34743926 pmcid: 8671346 doi: 10.1016/j.smim.2021.101511
Muzio L, Viotti A, Martino G. Microglia in neuroinflammation and neurodegeneration: from understanding to therapy. Front Neurosci. 2021;15:742065.
pubmed: 34630027 pmcid: 8497816 doi: 10.3389/fnins.2021.742065
Inoue Y, Trapnell BC, Tazawa R, Arai T, Takada T, Hizawa N, et al. Characteristics of a large cohort of patients with autoimmune pulmonary alveolar proteinosis in Japan. Am J Respir Crit Care Med. 2008;177(7):752–62.
pubmed: 18202348 pmcid: 2720118 doi: 10.1164/rccm.200708-1271OC
Trapnell BC, Nakata K, Bonella F, Campo I, Griese M, Hamilton J, et al. Pulmonary alveolar proteinosis. Nat Rev Dis Prim. 2019;5(1).
Uchida K, Nakata K, Suzuki T, Luisetti M, Watanabe M, Koch DE, et al. Granulocyte/macrophage-colony-stimulating factor autoantibodies and myeloid cell immune functions in healthy subjects. Blood. 2009;113(11):2547–56.
pubmed: 19282464 pmcid: 2656275 doi: 10.1182/blood-2008-05-155689
Anderson K, Carey B, Martin A, Roark C, Chalk C, Nowell-Bostic M, et al. Pulmonary alveolar proteinosis: an autoimmune disease lacking an HLA association. PLoS One. 2019;14(3):1–12.
doi: 10.1371/journal.pone.0213179

Auteurs

Shang-Yu Wang (SY)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.
Division of General Surgery, Department of Surgery, Chang Gung Memorial Hospital, Taoyuan, Taiwan.

Yu-Fang Lo (YF)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

Han-Po Shih (HP)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

Mao-Wang Ho (MW)

Division of Infectious Diseases, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan.

Chun-Fu Yeh (CF)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.
Division of Infectious Diseases, Department of Internal Medicine, Chang Gung Memorial Hospital, Taoyuan, Taiwan.

Jhan-Jie Peng (JJ)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

He-Ting Ting (HT)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

Kuo-Hsi Lin (KH)

Division of Infectious Diseases, Department of Internal Medicine, Tungs' Taichung MetroHarbor Hospital, Taichung, Taiwan.

Wen-Chi Huang (WC)

Division of Infectious Diseases, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan.

Yi-Chun Chen (YC)

Division of Infectious Diseases, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan.

Yu-Hsin Chiu (YH)

Division of Infectious Diseases, Department of Internal Medicine, Chi Mei Medical Center, Liouying, Tainan, Taiwan.

Chien-Wei Hsu (CW)

Department of Chest Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan.
School of Medicine, National Yang-Ming University, Taipei, Taiwan.

Yu-Ting Tseng (YT)

Section of Infectious Diseases, Department of Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan.

Lih-Shinn Wang (LS)

Division of Infectious Disease, Department of Internal Medicine, Buddhist Tzu Chi General Hospital and Tzu Chi University, Hualien, Taiwan.

Wei-Yi Lei (WY)

Department of Medicine, Hualien Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation and Tzu Chi University, Hualien, Taiwan.

Chen-Yuan Lin (CY)

Department of Hematology and Oncology, China Medical University Hospital, Taichung, Taiwan.
School of Pharmacy, China Medical University, Taichung, Taiwan.

Yu Aoh (Y)

Neuroscience Laboratory, Department of Neurology, China Medical University Hospital, Taichung, Taiwan.

Chia-Huei Chou (CH)

Division of Infectious Diseases, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan.

Tsai-Yi Wu (TY)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

Jing-Ya Ding (JY)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

Chia-Chi Lo (CC)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

You-Ning Lin (YN)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.

Kun-Hua Tu (KH)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.
Kidney Research Center, Department of Nephrology, Chang Gung Memorial Hospital, Taoyuan, Taiwan.

Wei-Te Lei (WT)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.
Section of Immunology, Rheumatology, and Allergy Department of Pediatrics, Hsinchu Mackay Memorial Hospital, Hsinchu City, Taiwan.

Chen-Yen Kuo (CY)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.
Division of Infectious Diseases, Department of Pediatrics, Chang Gung Memorial Hospital, Taoyuan city, Taiwan.

Chih-Yu Chi (CY)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan.
Division of Infectious Diseases, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan.
School of Medicine, College of Medicine, China Medical University, Taichung, Taiwan.

Cheng-Lung Ku (CL)

Laboratory of Human Immunology and Infectious Diseases, Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan. clku@cgu.edu.tw.
Department of Nephrology, Chang Gung Memorial Hospital, Taoyuan, Taiwan. clku@cgu.edu.tw.
Center for Clinical and Medical Immunology, Chang Gung University, Taoyuan, Taiwan. clku@cgu.edu.tw.

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