187
Views
2
CrossRef citations to date
0
Altmetric
REVIEW

Lipocalin 2 Participates in the Epidermal Differentiation and Inflammatory Processes of Psoriasis

ORCID Icon & ORCID Icon
Pages 2157-2166 | Published online: 31 Mar 2022

References

  • Boehncke WH, Schön MP. Psoriasis. Lancet. 2015;386(9997):983–994. doi:10.1016/S0140-6736(14)D61909-7
  • Cheng H, Xu M, Liu X, Zou X, Zhan N, Xia Y. TWEAK/Fn14 activation induces keratinocyte proliferation under psoriatic inflammation. Exp Dermatol. 2016;25(1):32–37. doi:10.1111/exd.12820
  • Rapalli VK, Waghule T, Gorantla S, Dubey SK, Saha RN, Singhvi G. Psoriasis: pathological mechanisms, current pharmacological therapies, and emerging drug delivery systems. Drug Discov Today. 2020;25(12):2212–2226. doi:10.1016/j.drudis.2020.09.023
  • Liu W, Zhang D, Luo M, et al. TNF-like weak inducer of apoptosis promotes angiogenesis, thereby exacerbating cutaneous psoriatic disease. J Invest Dermatol. 2021;141(5):1356–1360. doi:10.1016/j.jid.2020.09.023
  • Feldman SR, Goffe B, Rice G, et al. The challenge of managing psoriasis: unmet medical needs and stakeholder perspectives. Am Health Drug Benefits. 2016;9(9):504–513.
  • Hawkes JE, Chan TC, Krueger JG. Psoriasis pathogenesis and the development of novel targeted immune therapies. J Allergy Clin Immunol. 2017;140(3):645–653. doi:10.1016/j.jaci.2017.07.004
  • Skrzeczynska-Moncznik J, Wlodarczyk A, Zabieglo K, et al. Secretory leukocyte proteinase inhibitor-competent DNA deposits are potent stimulators of plasmacytoid dendritic cells: implication for psoriasis. J Immunol. 2012;189(4):1611–1617. doi:10.4049/jimmunol.1103293
  • Wang H, Wang S, Li L, et al. Involvement of the cytokine TWEAK in the pathogenesis of psoriasis vulgaris, pustular psoriasis, and erythrodermic psoriasis. Cytokine. 2021;138:155391. doi:10.1016/j.cyto.2020.155391
  • Gu H, Zhang Y, Zeng W, Xia Y. Participation of interferons in psoriatic inflammation. Cytokine Growth Factor Rev. 2021. doi:10.1016/j.cytogfr.2021.12.002
  • Gilet A, Zou F, Boumenir M, et al. Aldosterone up-regulates MMP-9 and MMP-9/NGAL expression in human neutrophils through p38, ERK1/2 and PI3K pathways. Exp Cell Res. 2015;331(1):152–163. doi:10.1016/j.yexcr.2014.11.004
  • Hwang ST, Nijsten T, Elder JT. Recent highlights in psoriasis research. J Invest Dermatol. 2017;137(3):550–556. doi:10.1016/j.jid.2016.11.007
  • Buonafine M, Martinez-Martinez E, Jaisser F. More than a simple biomarker: the role of NGAL in cardiovascular and renal diseases. Clin Sci. 2018;132(9):909–923. doi:10.1042/CS20171592
  • Shao S, Cao T, Jin L, et al. Increased lipocalin-2 contributes to the pathogenesis of psoriasis by modulating neutrophil chemotaxis and cytokine secretion. J Invest Dermatol. 2016;136(7):1418–1428. doi:10.1016/j.jid.2016.03.002
  • Sun WY, Bai B, Luo C, et al. Lipocalin-2 derived from adipose tissue mediates aldosterone-induced renal injury. JCI Insight. 2018;3(17):e120196. doi:10.1172/jci.insight.120196
  • Lee SA, Noel S, Kurzhagen JT, et al. CD4(+) T cell-derived NGAL modifies the outcome of ischemic acute kidney injury. J Immunol. 2020;204(3):586–595. doi:10.4049/jimmunol.1900677
  • Eilenberg W, Stojkovic S, Piechota-Polanczyk A, et al. Neutrophil gelatinase-associated lipocalin (NGAL) is associated with symptomatic carotid atherosclerosis and drives pro-inflammatory state in vitro. Eur J Vasc Endovasc Surg. 2016;51(5):623–631. doi:10.1016/j.ejvs.2016.01.009
  • Floderer M, Prchal-Murphy M, Vizzardelli C. Dendritic cell-secreted lipocalin 2 induces CD8+ T-cell apoptosis, contributes to T-cell priming and leads to a TH1 phenotype. PLoS One. 2014;9(7):e101881. doi:10.1371/journal.pone.0101881
  • Kamata M, Tada Y, Tatsuta A, et al. Serum lipocalin-2 levels are increased in patients with psoriasis. Clin Exp Dermatol. 2012;37(3):296–299. doi:10.1111/j.1365-2230.2011.04265.x
  • Matsuura T, Sato M, Nagai K, et al. Serum peptides as putative modulators of inflammation in psoriasis. J Dermatol Sci. 2017;87(1):36–49. doi:10.1016/j.jdermsci.2017.03.014
  • Sokolova MV, Simon D, Nas K, et al. A set of serum markers detecting systemic inflammation in psoriatic skin, entheseal, and joint disease in the absence of C-reactive protein and its link to clinical disease manifestations. Arthritis Res Ther. 2020;22(1):26. doi:10.1186/s13075-020-2111-8
  • Miao Q, Ku AT, Nishino Y, et al. Tcf3 promotes cell migration and wound repair through regulation of lipocalin 2. Nat Commun. 2014;5(1):4088. doi:10.1038/ncomms5088
  • Lee JH, Kye KC, Seo EY, et al. Expression of neutrophil gelatinase-associated lipocalin in calcium-induced keratinocyte differentiation. J Korean Med Sci. 2008;23(2):302–306. doi:10.3346/jkms.2008.23.2.302
  • Ku AT, Shaver TM, Rao AS, et al. TCF7L1 promotes skin tumorigenesis independently of β-catenin through induction of LCN2. eLife. 2017;6:e23242. doi:10.7554/eLife.23242
  • Abdel Hay R, Samir N, Safwat M, Rashed L, Soliman M. Tissue lipocalin-2 in psoriasis: is it a marker of metabolic disturbance or a possible marker of therapeutic efficacy after narrow band ultraviolet B? J Dermatolog Treat. 2020;31(5):519–523. doi:10.1080/09546634.2019.1605141
  • Wang D, Fang L, Pan G. Association of serum lipocalin-2 concentrations with psoriasis and psoriatic arthritis: an updated meta-analysis. Dis Markers. 2019;2019:7361826. doi:10.1155/2019/7361826
  • Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, Strong RK. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell. 2002;10(5):1033–1043. doi:10.1016/s1097-2765(02)00708-6
  • Klüber P, Meurer SK, Lambertz J, et al. Depletion of lipocalin 2 (LCN2) in mice leads to dysbiosis and persistent colonization with segmented filamentous bacteria. Int J Mol Sci. 2021;22(23):13156. doi:10.3390/ijms222313156
  • Qiu X, Macchietto MG, Liu X, et al. Identification of gut microbiota and microbial metabolites regulated by an antimicrobial peptide lipocalin 2 in high fat diet-induced obesity. Int J Obes. 2021;45(1):143–154. doi:10.1038/s41366-020-00712-2
  • Wang Q, Li S, Tang X, Liang L, Wang F, Du H. Lipocalin 2 protects against Escherichia coli infection by modulating neutrophil and macrophage function. Front Immunol. 2019;10:2594. doi:10.3389/fimmu.2019.02594
  • Watzenboeck ML, Drobits B, Zahalka S, et al. Lipocalin 2 modulates dendritic cell activity and shapes immunity to influenza in a microbiome dependent manner. PLoS Pathog. 2021;17(4):e1009487. doi:10.1371/journal.ppat.1009487
  • Lande R, Botti E, Jandus C, et al. The antimicrobial peptide LL37 is a T-cell autoantigen in psoriasis. Nat Commun. 2014;5(1):5621. doi:10.1038/ncomms6621
  • Mallbris L, O’Brien KP, Hulthén A, et al. Neutrophil gelatinase-associated lipocalin is a marker for dysregulated keratinocyte differentiation in human skin. Exp Dermatol. 2002;11(6):584–591. doi:10.1034/j.1600-0625.2002.110611.x
  • Howard JM, Nuguid JM, Ngole D, Nguyen H. Tcf3 expression marks both stem and progenitor cells in multiple epithelia. Development. 2014;141(16):3143–3152. doi:10.1242/dev.106989
  • Xu M, Zhang Y, Cheng H, et al. Transcription factor 7-like 1 dysregulates keratinocyte differentiation through upregulating lipocalin 2. Cell Death Discov. 2016;2(1):16028. doi:10.1038/cddiscovery.2016.28
  • Liu Y, Cheng H, Xiao S, Xia Y. A transcription factor 7-like 1-lipocalin 2 axis in the differentiation of keratinocytes. Cell Death Dis. 2016;7(6):e2241. doi:10.1038/cddis.2016.152
  • Kim HJ, Yoon HJ, Yoon KA, et al. Lipocalin-2 inhibits osteoclast formation by suppressing the proliferation and differentiation of osteoclast lineage cells. Exp Cell Res. 2015;334(2):301–309. doi:10.1016/j.yexcr.2015.03.008
  • Chung IH, Chen CY, Lin YH, et al. Thyroid hormone-mediated regulation of lipocalin 2 through the Met/FAK pathway in liver cancer. Oncotarget. 2015;6(17):15050–15064. doi:10.18632/oncotarget.3670
  • Hau CS, Kanda N, Tada Y, et al. Lipocalin-2 exacerbates psoriasiform skin inflammation by augmenting T-helper 17 response. J Dermatol. 2016;43(7):785–794. doi:10.1111/1346-8138.13227
  • Wolk K, Frambach Y, Jacobi A, et al. Increased levels of lipocalin 2 in palmoplantar pustular psoriasis. J Dermatol Sci. 2018;90(1):68–74. doi:10.1016/j.jdermsci.2017.12.018
  • Nelson AM, Zhao W, Gilliland KL, Zaenglein AL, Liu W, Thiboutot DM. Neutrophil gelatinase-associated lipocalin mediates 13-cis retinoic acid-induced apoptosis of human sebaceous gland cells. J Clin Invest. 2008;118(4):1468–1478. doi:10.1172/JCI33869
  • Colak S, Omma A, Sandikci SC, Yucel C, Omma T, Turhan T. Vaspin, neutrophil gelatinase-associated lipocalin and apolipoprotein levels in patients with psoriatic arthritis. Bratisl Lek Listy. 2019;120(1):65–69. doi:10.4149/BLL_2019_010
  • Chiricozzi A, Suárez-Fariñas M, Fuentes-Duculan J, et al. Increased expression of interleukin-17 pathway genes in nonlesional skin of moderate-to-severe psoriasis vulgaris. Br J Dermatol. 2016;174(1):136–145. doi:10.1111/bjd.14034
  • Shah M, Rennoll SA, Raup-Konsavage WM, Yochum GS. A dynamic exchange of TCF3 and TCF4 transcription factors controls MYC expression in colorectal cancer cells. Cell Cycle. 2015;14(3):323–332. doi:10.4161/15384101.2014.980643
  • Zhang X, Gao Y, Lu L, et al. JmjC domain-containing protein 6 (Jmjd6) derepresses the transcriptional repressor transcription factor 7-like 1 (Tcf7l1) and is required for body axis patterning during xenopus embryogenesis. J Biol Chem. 2015;290(33):20273–20283. doi:10.1074/jbc.M115.646554
  • Kuwahara A, Sakai H, Xu Y, Itoh Y, Hirabayashi Y, Gotoh Y. Tcf3 represses Wnt-β-catenin signaling and maintains neural stem cell population during neocortical development. PLoS One. 2014;9(5):e94408. doi:10.1371/journal.pone.0094408
  • Lories RJ, de Vlam K. Is psoriatic arthritis a result of abnormalities in acquired or innate immunity? Curr Rheumatol Rep. 2012;14(4):375–382. doi:10.1007/s11926-012-0257-3
  • Sakkas LI, Bogdanos DP. Are psoriasis and psoriatic arthritis the same disease? The IL-23/IL-17 axis data. Autoimmun Rev. 2017;16(1):10–15. doi:10.1016/j.autrev.2016.09.015
  • Boutet MA, Nerviani A, Gallo Afflitto G, Pitzalis C. Role of the IL-23/IL-17 axis in psoriasis and psoriatic arthritis: the clinical importance of its divergence in skin and joints. Int J Mol Sci. 2018;19(2):530. doi:10.3390/ijms19020530
  • Blauvelt A, Chiricozzi A. The immunologic role of IL-17 in psoriasis and psoriatic arthritis pathogenesis. Clin Rev Allergy Immunol. 2018;55(3):379–390. doi:10.1007/s12016-018-8702-3
  • Suzuki E, Mellins ED, Gershwin ME, Nestle FO, Adamopoulos IE. The IL-23/IL-17 axis in psoriatic arthritis. Autoimmun Rev. 2014;13(4–5):496–502. doi:10.1016/j.autrev.2014.01.050
  • Murakami M, Ohtake T, Horibe Y, et al. Acrosyringium is the main site of the vesicle/pustule formation in palmoplantar pustulosis. J Invest Dermatol. 2010;130(8):2010–2016. doi:10.1038/jid.2010.87
  • Wolk K, Wenzel J, Tsaousi A, et al. Lipocalin-2 is expressed by activated granulocytes and keratinocytes in affected skin and reflects disease activity in acne inversa/hidradenitis suppurativa. Br J Dermatol. 2017;177(5):1385–1393. doi:10.1111/bjd.15424
  • Turina MC, Landewé R, Baeten D. Lessons to be learned from serum biomarkers in psoriasis and IBD - The potential role in SpA. Expert Rev Clin Immunol. 2017;13(4):333–344. doi:10.1080/1744666X.2017.1244004
  • Ma JY, Shao S, Wang G. Antimicrobial peptides: bridging innate and adaptive immunity in the pathogenesis of psoriasis. Chin Med J. 2020;133(24):2966–2975. doi:10.1097/CM9.0000000000001240
  • Gul FC, Cicek D, Kaman D, Demir B, Nazik H. Changes of serum lipocalin-2 and retinol binding protein-4 levels in patients with psoriasis and Behçet’s disease. Eur J Dermatol. 2015;25(2):195–197. doi:10.1684/ejd.2014.2490
  • Baran A, Świderska M, Myśliwiec H, Flisiak I. Effect of psoriasis activity and topical treatment on serum lipocalin-2 levels. J Dermatolog Treat. 2017;28(2):136–140. doi:10.1080/09546634.2016.1180340
  • Romaní J, Caixàs A, Ceperuelo-Mallafré V, et al. Circulating levels of lipocalin-2 and retinol-binding protein-4 are increased in psoriatic patients and correlated with baseline PASI. Arch Dermatol Res. 2013;305(2):105–112. doi:10.1007/s00403-012-1306-5
  • El-Hadidi H, Samir N, Shaker OG, Otb S. Estimation of tissue and serum lipocalin-2 in psoriasis vulgaris and its relation to metabolic syndrome. Arch Dermatol Res. 2014;306(3):239–245. doi:10.1007/s00403-013-1414-x
  • Belstrøm D, Eiberg JM, Enevold C, et al. Salivary microbiota and inflammation-related proteins in patients with psoriasis. Oral Dis. 2020;26(3):677–687. doi:10.1111/odi.13277
  • Seo SJ, Ahn JY, Hong CK, et al. Expression of neutrophil gelatinase-associated lipocalin in skin epidermis. J Invest Dermatol. 2006;126(2):510–512. doi:10.1038/sj.jid.5700035
  • Ataseven A, Kesli R, Kurtipek GS, Ozturk P. Assessment of lipocalin 2, clusterin, soluble tumor necrosis factor receptor-1, interleukin-6, homocysteine, and uric acid levels in patients with psoriasis. Dis Markers. 2014;2014:541709. doi:10.1155/2014/541709
  • Wu G, Li H, Zhou M, et al. Mechanism and clinical evidence of lipocalin-2 and adipocyte fatty acid-binding protein linking obesity and atherosclerosis. Diabetes Metab Res Rev. 2014;30(6):447–456. doi:10.1002/dmrr.2493
  • Stejskal D, Karpísek M, Humenanska V, et al. Lipocalin-2: development, analytical characterization, and clinical testing of a new ELISA. Horm Metab Res. 2008;40(6):381–385. doi:10.1055/s-2008-1062746
  • El-Mesallamy HO, Hamdy NM, Sallam AA. Effect of obesity and glycemic control on serum lipocalins and insulin-like growth factor axis in type 2 diabetic patients. Acta Diabetol. 2013;50(5):679–685. doi:10.1007/s00592-012-0373-6
  • Aizawa N, Ishiuji Y, Tominaga M, et al. Relationship between the degrees of itch and serum lipocalin-2 levels in patients with psoriasis. J Immunol Res. 2019;2019:8171373. doi:10.1155/2019/8171373
  • Gulkesen A, Akgol G, Poyraz AK, et al. Lipocalin 2 as a clinical significance in rheumatoid arthritis. Cent Eur J Immunol. 2017;3(3):269–273. doi:10.5114/ceji.2017.70969
  • Chen L, Lin Z, Liu Y, et al. DZ2002 alleviates psoriasis-like skin lesions via differentially regulating methylation of GATA3 and LCN2 promoters. Int Immunopharmacol. 2021;91:107334. doi:10.1016/j.intimp.2020.107334
  • Baran A, Myśliwiec H, Kiluk P, Świderska M, Flisiak I. Serum irisin levels in patients with psoriasis. J Dermatolog Treat. 2017;28(4):304–308. doi:10.1080/09546634.2016.1254327
  • Xiao X, Yeoh BS, Vijay-Kumar M. Lipocalin 2: an emerging player in iron homeostasis and inflammation. Annu Rev Nutr. 2017;37(1):103–130. doi:10.1146/annurev-nutr-071816-064559
  • Watanabe K, Yoshino T, Takahashi M, et al. Clinical significance of neutrophil gelatinase-associated lipocalin and galectin-7 in tape-stripped stratum corneum of acne vulgaris. J Dermatol. 2018;45(5):618–621. doi:10.1111/1346-8138.14261
  • Nguyen VT, Farman N, Palacios-Ramirez R, et al. Cutaneous wound healing in diabetic mice is improved by topical mineralocorticoid receptor blockade. J Invest Dermatol. 2020;140(1):223–234.e227. doi:10.1016/j.jid.2019.04.030
  • Abdollahi M, Ng TS, Rezaeizadeh A, et al. Insulin treatment prevents wounding associated changes in tissue and circulating neutrophil MMP-9 and NGAL in diabetic rats. PLoS One. 2017;12(2):e0170951. doi:10.1371/journal.pone.0170951
  • Navrazhina K, Renert-Yuval Y, Frew JW, et al. Large-scale serum analysis identifies unique systemic biomarkers in psoriasis and hidradenitis suppurativa. Br J Dermatol. 2021. doi:10.1111/bjd.20642
  • Wang H, Xu Y, Jin M, Li H, Li S. miR-383 reduces keratinocyte proliferation and induces the apoptosis in psoriasis via disruption of LCN2-dependent JAK/STAT pathway activation. Int Immunopharmacol. 2021;96:107587. doi:10.1016/j.intimp.2021.107587
  • Akgül B, Bauer B, Zigrino P, Storey A, Mauch C, Pfister H. Upregulation of lipocalin-2 in human papillomavirus-positive keratinocytes and cutaneous squamous cell carcinomas. J Gen Virol. 2011;92(2):395–401. doi:10.1099/vir.0.025064-0
  • Takahashi T, Asano Y, Noda S, et al. A possible contribution of lipocalin-2 to the development of dermal fibrosis, pulmonary vascular involvement and renal dysfunction in systemic sclerosis. Br J Dermatol. 2015;173(3):681–689. doi:10.1111/bjd.13779
  • Lumsden KR, Nelson AM, Dispenza MC, et al. Isotretinoin increases skin-surface levels of neutrophil gelatinase-associated lipocalin in patients treated for severe acne. Br J Dermatol. 2011;165(2):302–310. doi:10.1111/j.1365-2133.2011.10362.x
  • Navrazhina K, Garcet S, Gonzalez J, Grand D, Frew JW, Krueger JG. In-depth analysis of the hidradenitis suppurativa serum proteome identifies distinct inflammatory subtypes. J Invest Dermatol. 2021;141(9):2197–2207. doi:10.1016/j.jid.2021.02.742